Evolution of the ribbon-like organization of the Golgi apparatus in animal cells.

The "ribbon," a structural arrangement in which Golgi stacks connect to each other, is considered to be restricted to vertebrate cells. Although ribbon disruption is linked to various human pathologies, its functional role in cellular processes remains unclear. In this study, we investigate the evolutionary origin of the Golgi ribbon. We observe a ribbon-like architecture in the cells of several metazoan taxa suggesting its early emergence in animal evolution predating the appearance of vertebrates. Supported by AlphaFold2 modeling, we propose that the evolution of Golgi reassembly and stacking protein (GRASP) binding by golgin tethers may have driven the joining of Golgi stacks resulting in the ribbon-like configuration. Additionally, we find that Golgi ribbon assembly is a shared developmental feature of deuterostomes, implying a role in embryogenesis. Overall, our study points to the functional significance of the Golgi ribbon beyond vertebrates and underscores the need for further investigations to unravel its elusive biological roles.

Deep-sea benthic crustacean and annelid data from the Bering Sea.

Samples of Crustacea and Annelida (Polychaeta, Sipuncula, and Hirudinea) were collected in the Bering Sea and the northwestern Pacific Ocean during scientific cruise SO-249 BERING in 2016. Biological samples were collected from 32 locations by the team on-board RV Sonne using a chain bag dredge at depths ranging between 330-5,070 m, and preserved in 96% ethanol. Specimens were morphologically identified to the lowest taxonomic level possible using a Leica M60 stereomicroscope. The generated data here comprise taxonomic information as well as annotated bathymetric and biogeographic information from a total of 78 samples (26 Crustacea, 47 Polychaeta, 4 Sipuncula, and 1 Hirudinea). The dataset was prepared following Darwin Core Biodiversity standards for FAIR data sharing based on Ocean Biodiversity Information System (OBIS) and Global Biodiversity Facility (GBIF) guidelines. The standardised digitised data were then mobilised to both OBIS and GBIF under CC BY 4.0 licence to publicly share and adopt the data. As records of these important marine taxa from bathyal and abyssal depths are sparse, especially from the deep Bering Sea, the herein generated and digitised data aid in filling existing knowledge gaps on their diversity and distribution in that region. As part of the "Biogeography of the NW Pacific deep-sea fauna and their possible future invasions into the Arctic Ocean" (BENEFICIAL) project, this dataset thus not only increases our knowledge in re-assessing and uncovering the deep-sea diversity of these taxa, but also serves policy and management sectors by providing first-hand data for global report assessments.

A New Model Organism to Investigate Extraocular Photoreception: Opsin and Retinal Gene Expression in the Sea Urchin Paracentrotus lividus.

Molecular research on the evolution of extraocular photoreception has drawn attention to photosensitive animals lacking proper eye organs. Outside of vertebrates, little is known about this type of sensory system in any other deuterostome. In this study, we investigate such an extraocular photoreceptor cell (PRC) system in developmental stages of the sea urchin Paracentrotus lividus. We provide a general overview of the cell type families present at the mature rudiment stage using single-cell transcriptomics, while emphasizing the PRCs complexity. We show that three neuronal and one muscle-like PRC type families express retinal genes prior to metamorphosis. Two of the three neuronal PRC type families express a rhabdomeric opsin as well as an echinoderm-specific opsin (echinopsin), and their genetic wiring includes sea urchin orthologs of key retinal genes such as hlf, pp2ab56e, barh, otx, ac/sc, brn3, six1/2, pax6, six3, neuroD, irxA, isl and ato. Using qPCR, in situ hybridization, and immunohistochemical analysis, we found that the expressed retinal gene composition becomes more complex from mature rudiment to juvenile stage. The majority of retinal genes are expressed dominantly in the animals' podia, and in addition to the genes already expressed in the mature rudiment, the juvenile podia express a ciliary opsin, another echinopsin, and two Go-opsins. The expression of a core of vertebrate retinal gene orthologs indicates that sea urchins have an evolutionarily conserved gene regulatory toolkit that controls photoreceptor specification and function, and that their podia are photosensory organs.

Run and hide: visual performance in a brittle star.

Spatial vision was recently reported in a brittle star, Ophiomastix wendtii, which lacks discrete eyes, but little is known about its visual ecology. Our aim was to better characterize the vision and visual ecology of this unusual visual system. We tested animal orientation relative to vertical bar stimuli at a range of angular widths and contrasts, to identify limits of angular and contrast detection. We also presented dynamic shadow stimuli, either looming towards or passing the animal overhead, to test for potential defensive responses. Finally, we presented animals lacking a single arm with a vertical bar stimulus known to elicit a response in intact animals. We found that O. wendtii orients to large (≥50 deg), high-contrast vertical bar stimuli, consistent with a shelter-seeking role and with photoreceptor acceptance angles estimated from morphology. We calculate poor optical sensitivity for individual photoreceptors, and predict dramatic oversampling for photoreceptor arrays. We also report responses to dark stimuli moving against a bright background - this is the first report of responses to moving stimuli in brittle stars and suggests additional defensive uses for vision in echinoderms. Finally, we found that animals missing a single arm orient less well to static stimuli, which requires further investigation.

Miniaturization of tardigrades (water bears): Morphological and genomic perspectives.

Tardigrades form a monophyletic group of microscopic ecdysozoans best known for surviving extreme environmental conditions. Due to their key phylogenetic position as a subgroup of the Panarthropoda, understanding tardigrade biology is important for comparative studies with related groups like Arthropoda. Panarthropods - and Ecdysozoa as a whole - likely evolved from macroscopic ancestors, with several taxa becoming secondarily miniaturized. Morphological and genomic evidence likewise points to a miniaturized tardigrade ancestor. The five-segmented tardigrade body typically measures less than 1 mm in length and consists of only about 1000 cells. Most organs comprise a relatively small number of cells, with the highest proportion belonging to the central nervous system, while muscles are reduced to a single cell each. Similarly, fully sequenced genomes of three tardigrade species - together with Hox gene expression data - point to extensive modifications, rearrangements, and major losses of genes and even a large body region. Parallels are evident with related ecdysozoans that may have also undergone genomic reductions, such as the nematode Caenorhabditis elegans. We interpret these data together as evidence of miniaturization in the tardigrade lineage, while cautioning that the effects of miniaturization may manifest in different ways depending on the organ or organ system under examination.

Recent thecideide brachiopods (Thecideida, Thecideoidea) from northern Sulawesi (Indonesia) with discovery of a new Thecidellina species (Thecidellinidae).

The scope of this paper concerns the species diversity of thecideide brachiopods living in the western Pacific equatorial region of Indonesia and the possibilities for circulation and dispersion of thecideide species along the coasts of Sulawesi and the Sea of Bali. The discovery of a new Thecidellina species, Thecidellina mawaliana sp. nov., adds a new genus to the Indonesian fauna. This species has a peculiar biogeography, different from those of Minutella cf. minuta (Cooper, 1981) and Ospreyella mutiara Simon Hoffman, 2013, other thecideides living together with the new species. Unfortunately, attempts to collect molecular sequence information from the specimens failed due to insufficient DNA preservation. Probable speciation mechanisms in this genus are discussed.

Detecting hybridization between sister species of Terebratulina (Brachiopoda, Cancellothyridoidea) in the North Atlantic: morphology versus molecules.

Investigating samples of the cancellothyridid brachiopod Terebratulina collected during the IceAGE (Me85/3) expedition of RV METEOR at the continental shelf around Iceland with both morphometrical and molecular methods, we were for the first time able to detect a hybridization event between brachiopod sister species, which are thought to have separated 60 MYA. Terebratulina retusa and T. septentrionalis can clearly be distinguished on the basis of consistent species-specific molecular signatures in both mitochondrial and nuclear markers, whereas morphometrical analyses proved to be less reliable for species determination than previously thought. Two out of 28 specimens were identified as offspring of a one-way hybridization event between T. retusa eggs and T. septentrionalis sperm. Whereas the fossil record of Terebratulina in the North Atlantic region is too fragmentary to reconstruct the history of the hybridization event, the different life history traits of the two species and current oceanographic conditions around Iceland offer plausible explanations for the occurrence of crossbreeds in this common brachiopod genus.

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.

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.

Revision of the brachiopod genus Amphithyris (Rhynchonelliformea: Platidiidae) with descriptions of two new species.

The recent brachiopod genus Amphithyris Thomson belongs to the family Platidiidae and to date comprises five species, A. seminula (Philippi, 1836), A. buckmani Thomson, 1918, A. hallettensis Foster, 1974, A. richardsonae Campbell & Fleming, 1981 and A. parva MacKinnon, Hiller, Long & Marshall, 2008. Like other platidiid genera, Amphithyris has a worldwide distribution, but is mainly found in the southern hemisphere, with the exception of A. seminula which occurs in the Mediterranean Sea. This study is the first revision of the genus Amphithyris. We describe two new species, A. cavernicola n. sp. from the Queensland Plateau, Coral Sea, Australia and A. comitodentis n. sp. from deep waters east of the South Island, New Zealand. A. cavernicola n. sp. represents the first record of the genus from Australian waters, whereas A. comitodentis n. sp. is the first species in the genus recorded from the deep sea. Additionally, we identified the type material of A. seminula in the brachiopod collection of the Museum für Naturkunde, Berlin and designated a lectotype for this species. Despite their simple shell morphology and few diagnostic features, we were able to clearly discriminate the (now) seven species by morphological (shell) characters such as absence/presence of a median septum, absence/presence of capillae, shell convexity and/or combinations of these. On the basis of all known records, the present distribution of Amphithyris spp. and a Cretaceous origin of the genus is discussed. 

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

INTRODUCTION: The 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. RESULTS: Using 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. CONCLUSION: Micro-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.

Linking micromorphism, brooding, and hermaphroditism in brachiopods: insights from Caribbean Argyrotheca (Brachiopoda).

In extant brachiopods, parental brooding of the larvae occurs exclusively within Rhynchonelliformea. Methods of larval protection range from simple retention of the larvae within the mantle cavity, to sophisticated brood care within highly specialized brood pouches found in Argyrotheca and Joania (Terebratulida, Megathyridoidea), Gwynia (Terebratulida, Gwynioidea), and all Thecideoidea (Thecideida). Previous studies on the reproductive biology of Argyrotheca yielded contrasting results on the epithelial origin of the brood pouches in this genus. Here, representatives of different species of Argyrotheca from the Belize Barrier Reef were examined using histological section series. Brood pouches of four species, A. cf. schrammi and Argyrotheca sp. 1-3, are of the same basic structure, formed by invaginations of the anterior body wall and connected to the visceral cavity via the metanephridia. The same four species are simultaneously hermaphroditic, suggesting that fertilization is achieved, at least partly, through selfing. One species, Argyrotheca rubrocostata, differs significantly from all others as it has no brood pouch and gonochoric gonads. Thus, the presence of brood pouches and simultaneous hermaphroditism are concluded to be correlated within Megathyridoidea and proposed to be homologous traits of Joania and several but not all species of Argyrotheca, questioning the monophyletic status of both genera. In contrast to the brood pouches of Thecideoidea, lophophoral epithelium is not involved in the formation of the pouches of Argyrotheca and Joania. Therefore, megathyridoid and thecideoid brood pouches are not homologous but evolved independently within rhynchonelliform brachiopods. All brachiopods with brood pouches share a micromorphic form and a short life span, limiting the space and time available for gamete and larval development. We suggest that the brood pouches and the hermaphroditic gonads of Argyrotheca spp. and Joania compensate these limitations by minimizing the loss of gametes and larvae, and by maximizing the chances of successful fertilization.

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 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. 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.

Phylogenetic analysis of freshwater sponges provide evidence for endemism and radiation in ancient lakes.

Morphologic and phylogenetic analysis of freshwater sponges endemic to lakes in Central Sulawesi, Siberia and South-East Europe is presented. We also analyzed several cosmopolitan sponge species from Eurasia and North America and included sponge sequences from public databases. In agreement with previous reports [Addis, J.S., Peterson, K.J., 2005. Phylogenetic relationships of freshwater sponges (Porifera, Spongillina) inferred from analyses of 18S rDNA, COI mtDNA, and ITS2 rDNA sequences. Zool. Scr. 34, 549-557], the metaniid sponge Corvomeyenia sp. was the most deeply branching species within a monophyletic lineage of the suborder Spongillina. Pachydictyum globosum (Malawispongiidae) and Nudospongilla vasta (Spongillidae), two morphologically quite distinct species from Sulawesi were found in a joint clade with Trochospongilla (Spongillidae) rendering Trochospongilla paraphyletic. Furthermore, Ochridaspongia sp., another Malawispongiidae, clustered far away from that clade, together with Ephydatia fluviatilis, making the latter family polyphyletic. The Lubomirskiidae endemic to Lake Baikal, Lubomirskia abietina, Baikalospongia bacillifera, B. intermedia, and Swartschewskia papyracea formed a well-supported clade that was most closely linked to the genus Ephydatia (99.9% identity over a total length of 2169 concatenated nucleotide positions). Our study indicates the frequent and independent origin of sponge species endemic to different freshwater ecosystems from a few cosmopolitan founder species. The highly specific primer sets newly developed here facilitate work on the molecular phylogeny and DNA barcoding of sponges.

Freshwater shrimp-sponge association from an ancient lake.

Shrimp-sponge associations occur frequently in marine ecosystems, serving as model systems for the evolution of eusociality. Here, we describe the first known instance of such association in freshwater from an ancient lake in Indonesia. The shrimp Caridina spongicola forms an exclusive and probably commensal association with a yet undescribed spongillinid sponge. Phylogenetic and ecological data suggest a comparatively recent origin of both taxa. Climatic fluctuations may have facilitated speciation and occasional hybridization of the shrimp species, which is derived from a rock-dwelling ancestor. Their extremely localized occurrence in an increasingly disturbed area makes both taxa a conservation priority.

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.