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Fine Structure of the Ventral Nerve Centre and Interspeciwc Identiwcation of Individual Neurons in the Enigmatic Chaetognatha

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Fine Structure of the Ventral Nerve Centre and Interspeciwc Identiwcation of Individual Neurons in the Enigmatic Chaetognatha Zoomorphology (2009) 128:53–73 DOI 10.1007/s00435-008-0074-4 ORIGINAL PAPER Fine structure of the ventral nerve centre and interspeciWc identiWcation of individual neurons in the enigmatic Chaetognatha SteVen Harzsch · Carsten H. G. Müller · Verena Rieger · Yvan Perez · Silvia Sintoni · Christian Sardet · Bill Hansson Received: 5 April 2008 / Accepted: 7 October 2008 / Published online: 21 November 2008 © The Author(s) 2008. This article is published with open access at Springerlink.com Abstract The enigmatic arrow worms (Chaetognatha) are to identify six diVerent types of neurons in the bilateral marine carnivores and among the most abundant planktonic somata clusters by means of the cytoplasmic composition organisms. Their phylogenetic position has been heavily (regarding the structure of the neurite and soma including debated for a long time. Most recent molecular studies still the shape and eu-/heterochromatin ratio within the nucleus) provide a diverging picture and suggest arrow worms to be as well as the size and position of these neurons. Further- some kind of basal protostomes. In an eVort to understand more, our study provides new insights into the neuropil the organization of the nervous system in this clade for a composition of the ventral nerve centre and several other broad comparison with other Metazoa we analysed the Wne structural features. Our second goal was to examine if ultrastructure of the ventral nerve centre in Spadella cepha- individually identiWable neurons are present in the ventral loptera by transmission electron microscopy. We were able nerve centres of four chaetognath species, Sagitta setosa, Sagitta enXata, Pterosagitta draco, and Spadella cephalop- tera. For that purpose, we processed whole mount speci- S. Harzsch (&) · C. H. G. Müller · V. Rieger · S. Sintoni · mens of these species for immunolocalization of RFamide- B. Hansson Department of Evolutionary Neuroethology, related neuropeptides and analysed them with confocal Max Planck Institute for Chemical Ecology, Beutenberg Campus, laser-scanning microscopy. Our experiments provide evi- Hans-Knöll-Street 8, 07745 Jena, Germany dence for the interspeciWc homology of individual neurons e-mail: [email protected] in the ventral nerve centres of these four chaetognath spe- cies suggesting that the potential to generate serially C. H. G. Müller Institut für Biowissenschaften, arranged neurons with individual identities is part of their Allgemeine und Spezielle Zoologie, Universität Rostock, ground pattern. Universitätsplatz 2, 18051 Rostock, Germany Keywords Spadella cephaloptera Y. Perez Ventral nerve centre · · Institut Méditerranéen d’Ecologie et de Paléoécologie, Pterosagitta draco · Sagitta spp. · Ultrastructure · UMR 6116 CNRS, “Persistence and Evolution Immunolocalization · Seriality · Neurophylogeny · Metazoa of the Biodiversity”, Université de Provence, 3 Place Victor Hugo Case 36, 13331 Marseille Cedex 3, France Introduction S. Sintoni Fakultät für Naturwissenschaften, The Chaetognatha (arrow worms) are transparent marine Institut für Neurobiologie und Sektion Biosystematische carnivores that range in length from 1 to 120 mm and are Dokumentation, Universität Ulm, 89081 Ulm, Germany among the most abundant planktonic organisms. The taxon C. Sardet comprises more than 120 species from all geographical and Bio Mar Cell, Laboratoire de Biologie du Développement, vertical ranges of the ocean (Shinn 1997; Nielsen 2001; UMR7009 CNRS/UPMC, Station Zoologique, Kapp 2007). Palaeontological evidence recently showed Observatoire Océanologique, 06234 Villefranche-sur-Mer Cedex, France chaetognaths to be present in the Early Cambrian (approx. 123 54 Zoomorphology (2009) 128:53–73 540–520 Myr ago) Chengjang biota (Vannier et al. 2007). concept in Arthropoda). Kutsch and Breidbach (1994) pre- These authors suggest placing them among the earliest sented a catalogue of features for examining cellular char- active predators and conclude that the ancestral chaetog- acteristics of individually identiWable neurons in order to naths were planktonic with possible ecological preferences explore whether they may be homologous between diVerent for hyperbenthic niches close to the sea bottom. The phylo- arthropod taxa. Their catalogue includes features such as genetic position of the chaetognaths within the Bilateria is the common ontogenetic origin of neurons, physiological heavily debated (review Harzsch and Müller 2007) and the criteria such as the characterization of a neuron as inhibi- most recent molecular studies provide a diverging picture. tory or excitatory, biochemical criteria such as the expres- By using Bayesian inference and maximum likelihood sion of speciWc neurotransmitters or neuron-speciWc method to analyse two broad phylogenomic datasets, Dunn markers, and morphological criteria such as the position of et al. (2008) suggest a sister-group relationship of Chaetog- the neuronal somata in relation to the ganglion framework natha to the Lophotrochozoa whereas Marlétaz et al. (2008) as well as the course of the neurites and the targets that they propose a most likely position of the Chaetognatha as a sis- innervate. Within the Protostomia, individually identiWable ter-group to all Protostomia. neurons have been shown to be present in the nervous sys- The ventral nerve centre of Chaetognatha is an elongate tems of, e.g. Arthropoda (Burrows 1996; Harzsch et al. structure lying between the epidermis and its basement 2005; Harzsch 2006), Annelida (Stuart et al. 1987; Huang membrane (reviewed in Harzsch and Müller 2007). This et al. 1998, Gilchrist et al. 1995; Brodfuehrer and Thoro- neuronal centre controls swimming by initiating contrac- good 2001; Orrhage and Müller 2005; Müller 2006), Nema- tions of the body wall musculature (Duvert et al. 1980; thelminthes/Cycloneuralia (White et al. 1986; Walthall Duvert and Barets 1983; Duvert and Savineau 1986) and 1995), basal Mollusca (Friedrich et al. 2002; Voronezhs- integrates mechanosensory input from the numerous ciliary kaya et al. 2002), Plathelminthes (Halton and Gustafsson fence receptors in the epidermis (Bone and Pulsford 1984; 1996; Reuter et al. 1998; Reuter and Halton 2001), and Bone and Goto 1991; Shinn 1997; Malakhov et al. 2005). It Gnathifera (Müller and Sterrer 2004). The presence of at consists of a central Wbrillar neuropil core, Xanked by lat- least some individually identiWable neurons in basal deuter- eral clusters of cell bodies and it is anteriorly connected to ostomes such as tunicates (Meinertzhagen 2004; Stach the brain by two main connectives (Bone and Pulsford 2005; Meinertzhagen et al. 2004; Imai and Meinertzhagen 1984; Goto and Yoshida 1987; Shinn 1997). The ventral 2007; Soviknes et al. 2007), and the lancelet (Wicht and nerve centre gives rise to a densely ramifying nervous Lacalli 2005) indicates that the potential to establish indi- plexus that provides motor innervation to the body muscu- vidual identities may not only be present in the ground pat- lature and innervates the ciliary fence receptors (Bone and tern of Protostomia; but may even date back to the ground Pulsford 1984). Some aspects of the Wne structure of the pattern of Bilateria. Our previous study on representatives ventral nerve centre have been analysed in several species of Sagitta had indicated the possibility that individually belonging to the genus Sagitta (Ahnelt 1980; Bone and identiWable neurons may also be present in Chaetognatha Pulsford 1984; Goto and Yoshida 1987; Bone and Goto (Harzsch and Müller 2007). The present contribution sets 1991). One goal of the present report is to provide further out to explore this question in more detail. insights into the ultrastructural characteristics of the ventral The tetrapeptide FMRFamide (Phe-Met-Arg-Phe-NH2) nerve centre and to compare these between representatives and FMRFamide-related peptides (FaRPs) form a large of Spadella and Sagitta. Furthermore, this Wne structural neuropeptide family with more than 50 members, all of analysis will serve as a background for a meaningful analy- which share the RFamide motif (reviews: Price and sis of the immunolocalization studies described below. Greenberg 1989; Greenberg and Price 1992; Walker 1992; Studies on the immunolocalization of RFamide-related Dockray 2004; Kriegsfeld 2006; Zajac and Mollereau neuropeptides emphasized serially arranged neurons in the 2006). This neuropeptide family is widely distributed ventral nerve centres of two arrow worm species, Sagitta among invertebrates and vertebrates and an increasing setosa (Müller, 1947) and Paraspadella gotoi (Casanova, amount of literature on the structural diversity and neuro- 1990) and suggested the presence of individually identiW- hormonal action of invertebrate FaRPs and other peptides, able neurons (Bone et al. 1987; Harzsch and Müller 2007; e.g. in Coelenterata (review Grimmelikhuijzen et al. 1992), Goto et al. 1992). The concept of individually identiWable Plathelminthes (review Fairweather and Halton 1991; Choi neurons is valid for the nervous systems of many proto- et al. 1996), Mollusca (review Muneoka and Kobayashi stome taxa. This means that neurons within the central ner- 1992), and Arthropoda (Keller 1992; Gaus et al. 1993; vous system can be treated as individuals that can be Groome 1993; Nässel 1993; Homberg 1994; Nässel and recognized from animal to animal of one species or even in Homberg 2006) highlights a growing appreciation of the individuals belonging to diVerent species that are more or importance of these substances. So far,
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