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Camera-type eyes in vertebrates and cephalopods are striking examples of parallel evolution of a complex structure. While comparisons have focused on these two groups, camera-type eyes with likely high functionality are also found in other invertebrate phyla with simpler brains. Employing single-cell RNA sequencing, we identify neurogenic cells in the adult eyes and brain of the marine annelid worm Platynereis dumerilii . Distinct neural stem cells in the camera-type adult eyes, located at the edge of the cup-shaped retina, and adjacent to the glass body/lens, produce radial lines of cells, reminiscent of stem cells in ciliary marginal zones of vertebrate eyes exhibiting life-long growth. Normal proliferation in the eye depends on ambient light, a phenomenon that depends on the integrity of the photoreceptor gene c-opsin1 , which is present in emerging rhabdomeric photoreceptors, and impacts on their differentiation. During reproductive maturation, proliferation in the eye as well as the entire brain sharply declines, while cells upregulate molecular characteristics of mammalian adult neural stem cell quiescence. Our data provide insights into the development and modulation of annelid head and brain cells, revealing similarities and differences to vertebrate eye development, neurogenesis and brain plasticity. Marine worms possess camera-type eyes. Here they show that the growth of marine annelid eyes depends on a stem cell system reminiscent of vertebrate eyes. Moreover, eye development seems to be tuned by a light-sensitive opsin known from vertebrate vision.

Background The annelid anterior central nervous system is often described to consist of a dorsal prostomial brain, consisting of several commissures and connected to the ventral ganglionic nerve cord via circumesophageal connectives. In the light of current molecular phylogenies, our assumptions on the primary design of the nervous system in Annelida has to be reconsidered. For that purpose we provide a detailed investigation of the adult nervous system of Magelonidae – a putatively basally branching annelid family - and studied early stages of the development of the latter. Results Our comparative investigation using an integrative morphological approach shows that the nervous system of Magelonidae is located inside the epidermis. The brain is composed of an anterior compact neuropil and posteriorly encircles the prostomial coelomic cavities. From the brain two lateral medullary cords branch off which fuse caudally. Prominent brain structures such as nuchal organs, ganglia or mushroom bodies are absent and the entire nervous system is medullary. Our investigations also contradict previous investigations and present an updated view on established assumptions and descriptions. Conclusion The comprehensive dataset presented herein enables a detailed investigation of the magelonid anterior central nervous system for the first time. The data reveal that early in annelid evolution complexity of brains and anterior sensory structures rises. Polymorphic neurons in clusters and distinct brain parts, as well as lateral organs - all of which are not present in outgroup taxa and in the putative magelonid sister group Oweniidae - already evolved in Magelonidae. Commissures inside the brain, ganglia and nuchal organs, however, most likely evolved in the stem lineage of Amphinomidae + Sipuncula and Pleistoannelida (Errantia+ Sedentaria). The investigation demonstrates the necessity to continuously question established descriptions and interpretations of earlier publications and the need for transparent datasets. Our results also hint towards a stronger inclusion of larval morphology and developmental investigations in order to understand adult morphological features, not only in Annelida.

An oral tradition for microRNA Recent work suggests that microRNAs, the ubiquitous, small, non-coding genetic elements with important regulatory roles, were important in the evolution of complexity in multicellular animals. What was the role of these microRNAs when they first evolved? A deep sequencing study of the marine ragworm Platynereis dumerilii , and comparison with other bilaterian animals, suggests that the most ancient known microRNA, miR-100, was initially active in neurosecretory cells around the mouth. Other highly conserved varieties were first present in specific tissues and organ systems, such as ciliated cells and parts of the nervous system, musculature and gut. This work suggests that the last common ancestor of bilaterian animals already had all these structures. Recent work suggests that microRNAs might have been important in the evolution of complexity in multicellular animals. Here it is shown that the most ancient known microRNA, miR–100, was initially active in neurosecretory cells around the mouth. Other highly conserved varieties were first present in specific tissues and organ systems. Thus, microRNA expression was initially restricted to an ancient set of ancient animal cell types and tissues. The spectacular escalation in complexity in early bilaterian evolution correlates with a strong increase in the number of microRNAs 1 , 2 . To explore the link between the birth of ancient microRNAs and body plan evolution, we set out to determine the ancient sites of activity of conserved bilaterian microRNA families in a comparative approach. We reason that any specific localization shared between protostomes and deuterostomes (the two major superphyla of bilaterian animals) should probably reflect an ancient specificity of that microRNA in their last common ancestor. Here, we investigate the expression of conserved bilaterian microRNAs in Platynereis dumerilii , a protostome retaining ancestral bilaterian features 3 , 4 , in Capitella , another marine annelid, in the sea urchin Strongylocentrotus , a deuterostome, and in sea anemone Nematostella , representing an outgroup to the bilaterians. Our comparative data indicate that the oldest known animal microRNA, miR-100, and the related miR-125 and let-7 were initially active in neurosecretory cells located around the mouth. Other sets of ancient microRNAs were first present in locomotor ciliated cells, specific brain centres, or, more broadly, one of four major organ systems: central nervous system, sensory tissue, musculature and gut. These findings reveal that microRNA evolution and the establishment of tissue identities were closely coupled in bilaterian evolution. Also, they outline a minimum set of cell types and tissues that existed in the protostome–deuterostome ancestor.

Animal bodies comprise diverse arrays of cells. To characterize cellular identities across an entire body, we have compared the transcriptomes of single cells randomly picked from dissociated whole larvae of the marine annelid Platynereis dumerilii. We identify five transcriptionally distinct groups of differentiated cells, each expressing a unique set of transcription factors and effector genes that implement cellular phenotypes. Spatial mapping of cells into a cellular expression atlas, and wholemount in situ hybridization of group-specific genes reveals spatially coherent transcriptional domains in the larval body, comprising, for example, apical sensory-neurosecretory cells versus neural/epidermal surface cells. These domains represent new, basic subdivisions of the annelid body based entirely on differential gene expression, and are composed of multiple, transcriptionally similar cell types. They do not represent clonal domains, as revealed by developmental lineage analysis. We propose that the transcriptional domains that subdivide the annelid larval body represent families of related cell types that have arisen by evolutionary diversification. Their possible evolutionary conservation makes them a promising tool for evo–devo research.

The bristle worm Platynereis dumerilii displays many interesting biological characteristics. These include its reproductive timing, which is synchronized to the moon phase, its regenerative capacity that is hormonally controlled, and a slow rate of evolution, which permits analyses of ancestral genes and cell types. As a marine annelid, Platynereis is also representative of the marine ecosystem, as well as one of the three large animal subphyla, the Lophotrochozoa. Here, we provide an overview of the molecular resources, functional techniques, and behavioral assays that have recently been established for the bristle worm. This combination of tools now places Platynereis in an excellent position to advance research at the frontiers of neurobiology, chronobiology, evo-devo, and marine biology.

For vision, insect and vertebrate eyes use rhabdomeric and ciliary photoreceptor cells, respectively. These cells show distinct architecture and transduce the light signal by different phototransductory cascades. In the marine ragworm Platynereis, we find both cell types: rhabdomeric photoreceptor cells in the eyes and ciliary photoreceptor cells in the brain. The latter use a photopigment closely related to vertebrate rod and cone opsins. Comparative analysis indicates that both types of photoreceptors, with distinct opsins, coexisted in Urbilateria, the last common ancestor of insects and vertebrates, and sheds new light on vertebrate eye evolution.

Signalling pathways are essential for the correct development of the central nervous system (CNS) in bilaterian animals. Here we show that in the CNS of the annelid Platynereis dumerilii , neural progenitor cells (NPCs) are located close to the ventral midline and express axin , a negative regulator of the Wnt/β-catenin pathway. Using pharmacological inhibitors, we observe that Wnt/β-catenin is required for the transition between proliferating NPCs and differentiating neurons. We also show that the Rho-associated kinase (Rok) is necessary for neurectoderm morphogenesis and ventral midline formation, and indirectly affects the distribution of the NPCs and the development of axonal scaffolds. Moreover, seven genes belonging to the planar cell polarity (PCP) pathway are expressed in the developing Platynereis neurectoderm, suggesting an involvement in its morphogenesis. When compared with previous studies in vertebrates, our data suggest that the involvement of the Wnt/β-catenin pathway in the control of neural cell proliferation/differentiation is ancestral to bilaterians. The Wnt/β-catenin pathway has important roles during neurogenesis in bilaterian animals. The authors show that this pathway regulates the transition from proliferating neural progenitors to differentiating neurons in the annelid Platynereis dumerilii , suggesting a conserved role in the last common bilaterian ancestor.

Background Diverse architectures of nervous systems (NSs) such as a plexus in cnidarians or a more centralized nervous system (CNS) in insects and vertebrates are present across Metazoa, but it is unclear what selection pressures drove evolution and diversification of NSs. One underlying aspect of this diversity lies in the cellular and molecular mechanisms driving neurogenesis, i.e. generation of neurons from neural precursor cells (NPCs). In cnidarians, vertebrates, and arthropods, homologs of SoxB and bHLH proneural genes control different steps of neurogenesis, suggesting that some neurogenic mechanisms may be conserved. However, data are lacking for spiralian taxa. Results To that end, we characterized NPCs and their daughters at different stages of neurogenesis in the spiralian annelid Capitella teleta. We assessed cellular division patterns in the neuroectoderm using static and pulse-chase labeling with thymidine analogs (EdU and BrdU), which enabled identification of NPCs that underwent multiple rounds of division. Actively-dividing brain NPCs were found to be apically-localized, whereas actively-dividing NPCs for the ventral nerve cord (VNC) were found apically, basally, and closer to the ventral midline. We used lineage tracing to characterize the changing boundary of the trunk neuroectoderm. Finally, to start to generate a genetic hierarchy, we performed double-fluorescent in-situ hybridization (FISH) and single-FISH plus EdU labeling for neurogenic gene homologs. In the brain and VNC, Ct-soxB1 and Ct-neurogenin were expressed in a large proportion of apically-localized, EdU+ NPCs. In contrast, Ct-ash1 was expressed in a small subset of apically-localized, EdU+ NPCs and subsurface, EdU− cells, but not in Ct-neuroD+ or Ct-elav1+ cells, which also were subsurface. Conclusions Our data suggest a putative genetic hierarchy with Ct-soxB1 and Ct-neurogenin at the top, followed by Ct-ash1, then Ct-neuroD, and finally Ct-elav1. Comparison of our data with that from Platynereis dumerilii revealed expression of neurogenin homologs in proliferating NPCs in annelids, which appears different than the expression of vertebrate neurogenin homologs in cells that are exiting the cell cycle. Furthermore, differences between neurogenesis in the head versus trunk of C. teleta suggest that these two tissues may be independent developmental modules, possibly with differing evolutionary trajectories.

Vestimentiferan tubeworms are representative species in deep-sea chemosynthetic ecosystems. Unlike most animals, these invertebrates lack mouths and digestive systems. Instead, their plumes function as the primary organ for direct metabolic exchange with the environment. Here, we present the single-cell transcriptome atlas of the Paraescarpia echinospica plume, offering single-cell resolution analysis for a deep-sea tubeworm. Our analysis revealed six cell clusters, namely hemocytes, proliferative cells, muscle cells, epithelial cells, nerve1 cells, and nerve2 cells, and we further characterized genes associated with immunity and transport. These findings establish a crucial foundation for future single-cell studies of tubeworms.