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Wollesen, T.

Publications and source records attributed to Wollesen, T..

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Early nervous system development in the chaetognath Spadella cephaloptera exhibits conserved bilaterian patterning features

Nervous systems display extensive diversity in structure and organization, yet a broadly conserved set of signaling pathway components and transcription factors is consistently associated with early neurogenesis in many animal lineages. Determining how these conserved markers map onto the spatiotemporal organization of neurogenic territories across phylogenetically informative but underrepresented lineages, particularly within Spiralia, is critical for refining inferences about the evolutionary origins and diversification of nervous systems. Chaetognaths, a spiralian lineage frequently recovered close to Gnathifera, have a compact and centralized nervous system but lack detailed molecular descriptions of early neural development. Here, we generate an expression-based developmental map of early neurogenesis in the chaetognath Spadella cephaloptera by combining nuclear-staining-based anatomical staging with spatiotemporal analyses of conserved developmental genes associated with early neurogenesis and axial patterning from gastrulation through early post-embryonic stages. Sce-soxB1-like1 and Sce-neuroD expressions mark a lateral neuroectodermal territory during gastrulation. Notably, Sce-neuroD is activated early in a broad ectodermal domain and is expressed within mitotically active neuroectodermal cells, consistent with early deployment in proliferative neurogenic territories. Sce-soxB1 and Sce-soxB2 show delayed and more spatially restricted expression relative to Sce-soxB1-like1, suggesting a paralog-specific partitioning of SoxB deployment during chaetognath neurogenesis. Sce-bmp2/4 and Sce-chd exhibit reciprocal dorsoventral expression during gastrulation that coincides with early neurogenic territory formation, before transitioning to more localized expression later in development. Sce-nk6 and Sce-hb9 reveal early ventral regionalization of the developing ventral nerve center (VNC), with Sce-hb9 occupying a subset of a broader Sce-nk6 domain, in line with conserved ventral subtype-associated regionalization. Sce-th (tyrosine hydroxylase) is detected in a small bilateral subset of hatchling VNC cells, while Sce-dbh (dopamine beta-hydroxylase) is first detected only in early juveniles in the anterior VNC and head domains, suggesting stage-dependent and region-specific deployment of catecholamine-pathway components. Together, these expression-based datasets provide a comparative reference for early neurogenesis in chaetognaths and a framework for assessing conserved and lineage-specific features of early neurogenic patterning across Spiralia.

evolutionary biology↗

Glycans in fertilization and adhesion: histochemical and ultrastructural insights from the chaetognath Spadella cephaloptera

BackgroundTo cope with strong and rapidly changing water currents, some marine invertebrates have evolved complex adhesive mechanisms that involve the interplay of different biomolecules, such as carbohydrates. Carbohydrates may, however, also be involved in other physiological processes such as reproduction, a research field poorly studied in protostomes. The benthic chaetognath Spadella cephaloptera is a protandric hermaphrodite capable of rapid attachment and detachment to substrates. Nevertheless, the putative underlying glycobiology during the adhesion process but also other physiological processes remain unknown for chaetognaths. MethodsIn the present study, through histological, immunohistochemical, and ultrastructural analysis, we characterized the location of different glycans in the reproductive and attachment systems of S. cephaloptera. Developmental changes of adhesive cells were investigated from early hatchlings up to adults. ResultsAcidic and sulfated mucosubstances were detected in the sperm ducts, whereas mature oocytes were surrounded by a carboxylated jelly coat. The distribution of adhesive cells in S. cephaloptera shifted from anterior discrete individual cells in hatchlings to posteriorly distributed cell clusters in the adult. Moreover, we identified secretion granules enriched in fibrous content inside the adhesive cells. Furthermore, immunohistochemistry revealed microtubule processes linking the adhesive cells to the intraepidermal plexus. Lectin affinity tests showed strong apical PNA binding and clear PHA-L/E and ConA signals in the adhesive cells. No evidence for a dual gland detachment system was observed. ConclusionsThis study provides the first glycan distribution analysis in a chaetognath, revealing the presence of carbohydrates in different structures of the reproductive system, highlighting their putative relevance during the fertilization process. Furthermore, the observed glycan moieties suggest that S. cephaloptera also combines convergently evolved features reported for other temporary attachment systems in marine invertebrates. However, S. cephaloptera also displays unique characters, such as specific ontogenetic changes occurring during early developmental stages that correspond to its feeding behavior. Our observations do not support the presence of additional gland cells mediating detachment. Finally, this work sets the framework for a molecular characterization of the reproductive and attachment systems of the enigmatic chaetognaths.

zoology↗

The anti-neural role of BMP signaling is a side effect of its global function in dorsoventral patterning

In Bilateria with centralized nervous systems (e.g. in vertebrates or arthropods), the minimum of the BMP signaling activity gradient defines the position of the central nervous system. BMP-dependent patterning of the secondary body axis is ancestral for Bilateria and possibly also for the bilaterian sister clade Cnidaria. However, the variety of levels of centralization of the nervous systems in Bilateria - from diffuse to fully centralized - as well as the lack of centralization of the nervous system in Cnidaria, suggest that BMP signaling cannot be perceived as a universally "anti-neural" signal. Here we use transgenic reporter lines in the anthozoan cnidarian Nematostella to show that BMP signaling is active in distinct neuronal populations. Moreover, attenuation of BMP signaling followed by RNA-Seq shows that BMP signaling is a positive regulator of many neuronal genes, including the top-tier neural progenitor marker soxB(2). Further, we analyze BMP signaling activity in the true jellyfish Aurelia and box jellyfish Tripedalia proving that BMP signaling in the diffuse cnidarian nervous system is not an anthozoan but an ancestral cnidarian feature, shared by anthozoans and medusozoans. Finally, we show that the highly centralized ventral nervous system of the non-model spiralian, the chaetognath Spadella, forms out of paired BMP signaling-positive domains on the lateral sides of the embryo. Together, our data suggest that one of the ancestral roles of BMP signaling was in promoting neurogenesis. We propose that the "anti-neural" function of BMP signaling in vertebrates and arthropods is a side effect of its global role in the dorsoventral patterning of the ectoderm.

developmental biology↗

Insights into adhesive and neuronal cell populations of the chaetognath Spadella cephaloptera using a single-nuclei transcriptomic atlas and genomic resources

To cope with extreme environmental conditions diverse marine species have developed mechanisms that allow them to permanently or temporarily attach to substrates. In the intertidal zone of marine habitats, where tidal ranges and currents may drift organisms away from their habitat, temporary adhesive systems such as the one inherent the arrow worm Spadella cephaloptera (Chaetognatha) constitute an essential trait for the survival of this taxon. The underlying molecular mechanism of this system has not been described yet, and the existing morphological information is limited to adults. Furthermore, a relationship between the nervous system and the attachment in S. cephaloptera remains to be demonstrated. In this study, single-nuclei sequencing of S. cephaloptera hatchlings was performed, using as a reference a newly sequenced and assembled genome to identify the transcriptomic profiles of the cells mediating attachment, neuronal populations, and the main cell types of chaetognath hatchlings. Our findings, supported by previous studies, suggest that the chaetognath adhesive system evolved convergently to those of other other metazoans. Moreover, diverse cell types were identified in the ventral nerve center and multiple ciliated cell types previously described from anatomical observations were validated. Ongoing in-depth investigation of these data, together with datasets from other developmental stages, will provide further insights into the evolutionary origins of the unique chaetognath body plan.

developmental biology↗

Chaetognaths exhibit the most extensive repertoire of Hox genes among protostomes.

1.The evolutionary origins and body plan diversification within bilaterians hinge on our understanding of conserved developmental gene networks across diverse taxa. While significant advances have been made in elucidating the anterior-posterior (AP) axis patterning across well-studied bilaterian lineages, our understanding of the conservation of AP-patterning gene expression in underexplored protostomes with a phylogenetically informative position remains limited. Chaetognaths, a group of marine invertebrates, form a clade with Gnathifera as a sister to the remaining Lophotrochozoa, occupying an early-diverging branch of the spiralian lineage. Their phylogenetic position provides potentially valuable evolutionary insights into whether the AP patterning reflects conserved bilaterian mechanisms or reveals distinct lineage-specific adaptations. Here, we investigate the expression patterns of anterior nervous system markers (otx, nk2.1, six3/6) and Hox genes in post-embryonic stages of the chaetognath Spadella cephaloptera using fluorescence whole-mount in situ hybridization. We identify expression domains of anterior-patterning genes in the cerebral ganglion and head structures, consistent with their conserved role in anterior central nervous system (CNS) specification in bilaterians. Additionally, we describe a staggered expression pattern of Hox genes, including previously undescribed central (Sce-med6) and posterior class (Sce-postC and Sce-postD), along the ventral nerve cord (VNC) and post-anal tail. Our results demonstrate that chaetognaths exhibit the most extensive repertoire of Hox genes among protostomes, within metazoans only surpassed by chordates. All AP patterning genes are expressed in a staggered manner, with Hox gene expression absent in the head region. This pattern resembles the conserved expression profile inferred for the last common bilaterian ancestor and is only rudimentarily visible in other spiralians, including annelids and mollusks. Posterior Hox genes including the newly discovered postC and postD genes are absent in the hitherto investigated gnathiferan sister groups such as rotifers. The absence of a postanal tail in rotifers and other gnathiferans, combined with the expression of posterior Hox genes in the elongated postanal tail region, suggests their involvement in the formation of this unique chaetognath structure. Posterior flexibility of Hox genes, as previously hypothesized for chordates, likely contributed to the formation of the chaetognath tail during the early Cambrian period.

developmental biology↗

Characterization of eyes, photoreceptors and opsins in developmental stages of the chaetognath Spadella cephaloptera

The phylogenetic position of chaetognaths has been debated for decades, however recently they have been grouped into the Gnathifera, sister taxon to the Lophotrochozoa. Chaetognaths possess photoreceptor cells that are anatomically unique and arranged remarkably different in the eyes of the various species. Studies investigating eye development and underlying gene regulatory networks are so far missing. In order to gain insights into the development and the molecular toolkit of chaetognath photoreceptors and eyes a new transcriptome of the epibenthic species Spadella cephaloptera was searched for opsins. Our screen revealed single-copies of xenopsin and peropsin and gene expression analyses demonstrated that only xenopsin is expressed in photoreceptor cells of the developing lateral eyes. Adults likewise exhibit two xenopsin+ photoreceptor cells in each of their lateral eyes. Beyond that, a single cryptochrome gene was uncovered and found co-expressed with xenopsin in some photoreceptor cells of the lateral developing eye. In addition, it is co-expressed with peropsin in the cerebral ganglia, a condition reminiscent of a non-visual photoreceptive zone in the apical nervous system of the annelid Platynereis dumerilii that performs circadian entrainment and melatonin release. Cryptochrome expression was also detected in cells of the corona ciliata, a circular organ in the posterior dorsal head region that has been attributed several functions arguing for an involvement of this organ in circadian entrainment. Our study demonstrates the importance to investigate representatives of the Gnathifera, a clade that has been neglected with respect to developmental studies and that might contribute to unravel the evolution of spiralian and bilaterian body plans.

zoology↗

The quagga mussel genome and the evolution of freshwater tolerance

European freshwater dreissenid mussels evolved from marine ancestors during the Miocene approximately 30 million years ago and today include some of the most successful and destructive invasive invertebrate species of temperate freshwater environments. Here we sequenced the genome of the quagga mussel Dreissena rostriformis to identify evolutionary adaptations involved in embryonic osmoregulation. We found high gene expression levels of a novel subfamily of lophotrochozoan-specific aquaporin water channel, a vacuolar ATPase and a sodium/hydrogen exchanger during early cleavage, a period defined by the formation of inter-cellular fluid-filled cleavage cavities. Independent expansions of the lophotrochoaquaporin clade that coincide with at least five independent colonisation events of freshwater environments confirm their central role in freshwater adaptation. The pattern of repeated aquaporin expansion and the evolution of membrane-bound fluid-filled osmoregulatory structures in diverse taxa points to a fundamental principle guiding the evolution of freshwater tolerance that may provide a framework for future efforts towards invasive species control.

genomics↗