Patrick Beckers

The Nervous Systems of Basally Branching Nemertea (Palaeonemertea)

In recent years, a lot of studies have been published dealing with the anatomy of the nervous system in different spiralian species. The only nemertean species investigated in this context probably shows derived characters and thus the conditions found there are not useful in inferring the relationship between nemerteans and other spiralian taxa. Ingroup relationships within Nemertea are still unclear, but there is some agreement that the palaeonemerteans form a basal, paraphyletic grade. Thus, palaeonemertean species are likely the most informative when comparing with other invertebrate groups. We therefore analyzed the nervous system of several palaeonemertean species by combining histology and immunostaining. 3D reconstructions based on the aligned slices were performed to get an overall impression of the central nervous system, and immunohistochemistry was chosen to reveal fine structures and to be able to compare the data with recently published results. The insights presented here permit a first attempt to reconstruct the primary organization of the nemertean nervous system. This comparative analysis allows substantiating homology hypotheses for nerves of the peripheral nervous system. This study also provides evidence that the nemertean brain primarily consists of two lobes connected by a strong ventral commissure and one to several dorsal commissures. During nemertean evolution, the brain underwent continuous compartmentalization into a pair of dorsal and ventral lobes interconnected by commissures and lateral tracts. Given that this conclusion can be corroborated by cladistic analyses, nemerteans should share a common ancestor with spiralians that primarily have a simple brain consisting of paired medullary, frontally commissurized and reinforced cords. Such an organization resembles the situation found in presumably basally branching annelids or mollusks.

Lophotrochozoan neuroanatomy: An analysis of the brain and nervous system of Lineus viridis(Nemertea) using different staining techniques.

BackgroundThe now thriving field of neurophylogeny that links the morphology of the nervous system to early evolutionary events relies heavily on detailed descriptions of the neuronal architecture of taxa under scrutiny. While recent accounts on the nervous system of a number of animal clades such as arthropods, annelids, and molluscs are abundant, in depth studies of the neuroanatomy of nemerteans are still wanting. In this study, we used different staining techniques and confocal laser scanning microscopy to reveal the architecture of the nervous system of Lineus viridis with high anatomical resolution.ResultsIn L. viridis, the peripheral nervous system comprises four distinct but interconnected nerve plexus. The central nervous system consists of a pair of medullary cords and a brain. The brain surrounds the proboscis and is subdivided into four voluminous lobes and a ring of commissural tracts. The brain is well developed and contains thousands of neurons. It does not reveal compartmentalized neuropils found in other animal groups with elaborate cerebral ganglia.ConclusionsThe detailed analysis of the nemertean nervous system presented in this study does not support any hypothesis on the phylogenetic position of Nemertea within Lophotrochozoa. Neuroanatomical characters that are described here are either common in other lophotrochozoan taxa or are seemingly restricted to nemerteans. Since detailed descriptions of the nervous system of adults in other nemertean species have not been available so far, this study may serve as a basis for future studies that might add data to the unsettled question of the nemertean ground pattern and the position of this taxon within the phylogenetic tree.

The future of nemertean taxonomy (phylum Nemertea) — a proposal

Submitted: 15 January 2016 Accepted: 6 March 2016 doi:10.1111/zsc.12182 Sundberg, P., Andrade, S.C.S., Bartolomaeus, T., Beckers, P., von D€ ohren, J., Kr€amer, D., Gibson, R., Giribet, G., Herrera-Bachiller, A., Juan, J., Kajihara, H., Kvist, S., K anneby, T., Sun S.-C., Thiel, M., Turbeville, J.M. , Strand, M. (2016). The future of nemertean taxonomy (phylum Nemertea) — a proposal. —Zoologica Scripta, 45: 579–582. Corresponding author: Per Sundberg, University of Gothenburg, Department of Marine Sciences, Gothenburg, Sweden. E-mail: per.sundberg@gu.se Per Sundberg, University of Gothenburg, Department of Marine Sciences, Gothenburg, Sweden.. E-mail: per.sundberg@gu.se S onia C. S. Andrade, Departamento de Gen etica e Biologia Evolutiva, IB-Universidade de, S~ao Paulo, Brazil, S~ao Paulo, Brazil. E-mail: soniacsandrade@gmail.com Thomas Bartolomaeus, Patrick Beckers, J€orn von D€ohren, and Daria Kr€amer, University of Bonn, Institute of Evolutionary Biology and Animal Ecology, Bonn, Germany. E-mails: tbartolomaeus@evolution.uni-bonn.de, pbeckers@evolution.uni-bonn.de, jdoehren@evolution.uni-bonn.de, dkraemer@evolution.uni-bonn.de Ray Gibson, 94 Queens Avenue, Meols, Wirral, CH47 0NA, U.K. E-mail: bfginc@hotmail.co.uk Gonzalo Giribet, Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. E-mail: ggiribet@g.harvard.edu Alfonso Herrera-Bachiller, and Juan Junoy, Departamento de Ciencias de la Vida, Universidad de Alcal a, Madrid, Spain. E-mails: alfonso@herrerabachiller.com, juan.junoy@uah.es Hiroshi Kajihara, Faculty of Science, Hokkaido University, Sapporo, Japan. E-mail: kazi@mail.sci.hokudai.ac.jp Sebastian Kvist, Department of Natural History, Royal Ontario Museum, Toronto, Canada and Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada. E-mail: sebastian.kvist@utoronto.ca Tobias K anneby, Swedish Museum of Natural History, Department of Zoology, Stockholm, Sweden. E-mail: Tobias.Kanneby@nrm.se, tobiaskanneby@gmail.com Shi-Chun Sun, Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, China. E-mail: sunsc@ouc.edu.cn Martin Thiel, Facultad Ciencias del Mar, Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Universidad Cat olica del Norte, Coquimbo, Chile. E-mail: thiel@ucn.cl James M. Turbeville, Department of Biology, Virginia Commonwealth University, Richmond, VA, USA. E-mail: jmturbeville@vcu.edu Malin Strand, Swedish Species Information Centre, The Sven Lov en Centre for Marine Sciences, Str€omstad, Sweden. E-mail: malin.strand@slu.se

The nervous systems of Pilidiophora (Nemertea)

Today molecular data recover three higher taxa in nemerteans, Palaeonemertea, Pilidiophora and Hoplonemertea. Hubrechtella dubia, a former palaeonemertean taxon was excluded from palaeonemerteans and is now supported as the sister group to heteronemerteans. This taxon is called Pilidiophora, because H. dubia and Heteronemertea share a pilidium larva. To find additional morphological evidence for Pilidiophora, the nervous system of 13 species of this taxon were investigated using different histological techniques. The central or medullated nervous system of nemerteans consists of a ring-shaped brain and lateral branching medullary cords. While the brain of basally branching nemerteans shows no or only slightly posterior enlargement, the brain of Pilidiophora expands caudally. Pilidiophora possess a conspicuous sensory organ, the cerebral organ. Although this organ is also found in hoplonemerteans and certain palaeonemertean species, only in Pilidiophora this organ is directly connected to the dorsal lobe of the brain. Additionally, this organ terminates in a layer of neurons close to the blood vessel in all pilidiophoran species. The analysis indicates that although in H. dubia some characters of the nervous system show the plesiomorphic state, the morphology of the cerebral organ provides an apomorphic character for a taxon Pilidiophora.

Early evolution of radial glial cells in Bilateria

Bilaterians usually possess a central nervous system, composed of neurons and supportive cells called glial cells. Whereas neuronal cells are highly comparable in all these animals, glial cells apparently differ, and in deuterostomes, radial glial cells are found. These particular secretory glial cells may represent the archetype of all (macro) glial cells and have not been reported from protostomes so far. This has caused controversial discussions of whether glial cells represent a homologous bilaterian characteristic or whether they (and thus, centralized nervous systems) evolved convergently in the two main clades of bilaterians. By using histology, transmission electron microscopy, immunolabelling and whole-mount in situ hybridization, we show here that protostomes also possess radial glia-like cells, which are very likely to be homologous to those of deuterostomes. Moreover, our antibody staining indicates that the secretory character of radial glial cells is maintained throughout their various evolutionary adaptations. This implies an early evolution of radial glial cells in the last common ancestor of Protostomia and Deuterostomia. Furthermore, it suggests that an intraepidermal nervous system—composed of sensory cells, neurons and radial glial cells—was probably the plesiomorphic condition in the bilaterian ancestor.

Phylogenetic significance of chaetal arrangement and chaetogenesis in Maldanidae (Annelida)

Chaetae are important structures to facilitate locomotion in annelids. Being at the interface between the organisms and its environment, chaetae are supposed to underlie strong functional constraints to optimize the relation between structure and function. As such chaetae are potentially susceptible for convergent evolution. On the other hand, chaetae gained enormous taxonomic importance due to their conservative structure in species and supraspecific taxa which reasonably can only be explained by strong evolutionary constrains that conserve their structure. In this paper, we study the chaetation and chaetogenesis in two species of Maldanidae, Clymenura clypeata Saint-Joseph 1894 and Johnstonia clymenoides Quatrefages 1866 to unravel conservative traits in their structure and development. In a literature survey across maldanids, we address questions on the ontogenetic variation, on homology and on the phylogenetic significance especially of the bearded hooked neurochaetae. We provide evidence that functionally constraint ontogenetic variation overlies historically (phylogenetically) constraint expression of structural information and can show that within maldanids a variety of different chaetal types must be homologous due to their ontogenetic continuity. Furthermore, we use chaetation and chaetal characters to discuss the subgroup relationships within Maldanomorpha in the light of recent cladistics analyses based on morphological and molecular data. This study shows that functional considerations need to use phylogenies as backbone.

Myoanatomy and anterior muscle regeneration of the fireworm Eurythoe cf. complanata (Annelida: Amphinomidae)

Amphinomidae or so‐called “fireworms” are known for their inflammatory substances and their regeneration ability. Recent transcriptome‐based molecular analyses revealed that these remarkable annelids are a basal branching taxon outside the annelid main radiation (Pleistoannelida). Although several studies dealing with analyses of the morphology of these annelids have been published, detailed investigations of the anterior muscle regeneration and the musculature in general are largely lacking for amphinomids. Using histology, phalloidin labeling together with subsequent confocal laser scanning microscopy (cLSM), and further light microscopic image acquisition of different regeneration stages, we here present the first morphological study describing the myoanatomy and muscular regeneration. During anterior muscular regeneration, longitudinal muscle bundles develop prior to transverse muscle fibers and segment boundaries. Additionally, Eurythoe cf. complanata develops an independent muscular ring surrounding the mouth opening in an early stage of regeneration. Detailed investigation of adult body wall musculature and the parapodial muscle complex in amphinomids show that E. cf. complanata bears well‐developed dorsal and ventral longitudinal muscle bundles as well as outer transverse muscles comparable to the pattern described for several Pleistoannelida. Furthermore, the biramous parapodia possess a complex meshwork of distinct muscle fibers allowing detailed comparisons with other annelid families. J. Morphol. 277:306–315, 2016.

On the role of the proventricle region in reproduction and regeneration in Typosyllis antoni (Annelida: Syllidae)

BackgroundSyllids are a species rich annelid family possessing remarkable regenerative ability, which is not only the response after traumatic injury, but also a key step during the life cycle of several syllid taxa. In these animals the posterior part of the body becomes an epitoke and is later detached as a distinct unit named stolon. Such a sexual reproductive mode is named schizogamy or stolonization. The prostomium and the proventricle, a modified foregut structure, have been proposed to have a control function during this process, though the concrete mechanisms behind it have never been elucidated.ResultsBy using different experimental set-ups, histology and immunohistochemistry combined with subsequent cLSM analyzes, we investigate and document the regeneration and stolonization in specimens of Typosyllis antoni that were amputated at different levels throughout the antero-posterior body axis. The removal of the anterior end including the proventricle implies an incomplete anterior regeneration as well as severe deviations from the usual reproductive pattern, i.e. accelerated stolonization, masculinization and the occurrence of aberrant stolons. The detailed anatomy of aberrant stolons is described. A histological study of the proventricle revealed no signs of glandular or secretory structures. The ventricle and the caeca are composed of glandular tissue but they are not involved in the reproductive and regenerative processes.ConclusionsAs in other investigated syllids, the proventricle region has a significant role during stolonization and reproduction processes in Typosyllis antoni. When the proventricle region is absent, anterior and posterior regeneration are considerably deviated from the general patterns. However, proventricle ultrastructure does not show any glandular component, thereby questioning a direct involvement of this organ itself in the control of reproduction and regeneration. Our findings offer a comprehensive starting point for further studies of regeneration and reproductive control in syllids as well as annelids in general.

Observations and Experiments on the Biology and Life History of Riseriellus occultus (Heteronemertea: Lineidae)

Studies on the biology and life history of nemerteans are scarce, mostly because these animals are nocturnal. In order to broaden the knowledge base on the life history of nemerteans as a prerequisite for comparative analyses, we studied a population of Riseriellus occultus (Heteronemertea: Lineidae) inhabiting the rocky intertidal in southern Brittany near Concarneau (France) for more than 10 years. Our studies show that R. occultus is an iteroparous, perennial species exclusively inhabiting rocky shore crevices that result from onionskin weathering of the granite. From September through October R. occultus reproduces by external fertilization and develops via a planktonic pilidium larva, which, under laboratory conditions, metamorphoses after about six weeks. Adults of R. occultus are nocturnal macrophagous predators that preferentially feed on the gastropods Gibbula umbilicalis and Patella species, but also consume the bivalve Mytilus edulis. Since R. occultus devours the snail inside the shell, we fixed individuals while feeding, and serially sectioned them. Reconstruction of the sections shows that R. occultus swallows the entire soft body and finally detaches the columellar muscle from the shell. Estimates on the density of R. occultus inside the rock crevices provide evidence for clustered distribution and locally high abundance on the rocky shore. These data strongly suggest that R. occultus affects the structure of the rocky shore gastropod community. Although our data are still fragmentary with respect to the ecology of this species and its role in the local food web, our knowledge has grown to such extent that R. occultus can now be regarded as one of the few well characterized nemertean species.

Comparative sperm ultrastructure in Nemertea

Although the monophyly of Nemertea is strongly supported by unique morphological characters and results of molecular phylogenetic studies, their ingroup relationships are largely unresolved. To contribute solving this problem we studied sperm ultrastructure of 12 nemertean species that belong to different subtaxa representing the commonly recognized major monophyletic groups. The study yielded a set of 26 characters with an unexpected variation among species of the same genus (Tubulanus and Procephalothrix species), whereas other species varied in metric values or only one character state (Ramphogordius). In some species, the sperm nucleus has grooves (Zygonemertes virescens, Amphiporus imparispinosus) that may be twisted and give a spiral shape to the sperm head (Paranemertes peregrina, Emplectonema gracile). To make the characters from sperm ultrastructure accessible for further phylogenetic analyses, they were coded in a character matrix. Published data for eight species turned out to be sufficiently detailed to be included. Comparative evaluation of available information on the sperm ultrastructure suggests that subtaxa of Heteronemertea and Hoplonemertea are supported as monophyletic by sperm morphology. However, the data do not provide information on the existing contradictions regarding the internal relationships of “Palaeonemertea.” Nevertheless, our study provides evidence that sperm ultrastructure yields numerous potentially informative characters that will be included in upcoming phylogenetic analyses. J. Morphol. 2010.