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      The early development of the onychopod cladoceran Bythotrephes longimanus (Crustacea, Branchiopoda)

      research-article
      1 , 2 , , 1 ,
      Frontiers in Zoology
      BioMed Central
      Cell lineage, Cladocera, Crustacea, Development, Cleavage pattern

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          Abstract

          Introduction

          Within arthropods, several crustacean groups are unique in their early development due to their stereotyped cell division patterns and cell lineages. However, it is still unclear whether these cell division patterns are homologous between the various crustacean groups and whether they could indicate the ground pattern of Tetraconata (Crustacea and Hexapoda). In this study we describe the early development of the raptorial water flea Bythotrephes longimanus as a representative of the Cladocera within branchiopods.

          Results

          In B. longimanus the early cell lineage and the cell division pattern are stereotyped up to the fifth cell division cycle. As a morphological marker a nurse cell remnant ( ncr) identifies the cell lineage of the smallest and division delayed blastomere up to the 16-cell stage. This marker might be indicative of the germ line. By combining histology, confocal laser scanning microscopy, and 4D microscopy, we reconstruct the early cell lineage and cell division pattern and follow transient formations of cell morphological structures in their temporal and spatial behavior up to gastrulation.

          Conclusions

          Correspondences to the early cleavage pattern of other Cladocera suggest that the described pattern can be assumed to be ancestral for either the entire Cladocera or for the majority of the Cladocera comprising Anomopoda, Ctenopoda and Onychopoda. The comparison to the cell division patterns of other crustacean groups such as Malacostraca, Ostracoda, and Copepoda reveals similarities that allow for a discussion of a common pattern for the crustacean groups and a ground pattern for the Tetraconata.

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          Most cited references34

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          Mechanisms of germ cell specification across the metazoans: epigenesis and preformation.

          Germ cells play a unique role in gamete production, heredity and evolution. Therefore, to understand the mechanisms that specify germ cells is a central challenge in developmental and evolutionary biology. Data from model organisms show that germ cells can be specified either by maternally inherited determinants (preformation) or by inductive signals (epigenesis). Here we review existing data on 28 metazoan phyla, which indicate that although preformation is seen in most model organisms, it is actually the less prevalent mode of germ cell specification, and that epigenetic germ cell specification may be ancestral to the Metazoa.
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            Pancrustacean phylogeny in the light of new phylogenomic data: support for Remipedia as the possible sister group of Hexapoda.

            Remipedes are a small and enigmatic group of crustaceans, first described only 30 years ago. Analyses of both morphological and molecular data have recently suggested a close relationship between Remipedia and Hexapoda. If true, the remipedes occupy an important position in pancrustacean evolution and may be pivotal for understanding the evolutionary history of crustaceans and hexapods. However, it is important to test this hypothesis using new data and new types of analytical approaches. Here, we assembled a phylogenomic data set of 131 taxa, incorporating newly generated 454 expressed sequence tag (EST) data from six species of crustaceans, representing five lineages (Remipedia, Laevicaudata, Spinicaudata, Ostracoda, and Malacostraca). This data set includes all crustacean species for which EST data are available (46 species), and our largest alignment encompasses 866,479 amino acid positions and 1,886 genes. A series of phylogenomic analyses was performed to evaluate pancrustacean relationships. We significantly improved the quality of our data for predicting putative orthologous genes and for generating data subsets by matrix reduction procedures, thereby improving the signal to noise ratio in the data. Eight different data sets were constructed, representing various combinations of orthologous genes, data subsets, and taxa. Our results demonstrate that the different ways to compile an initial data set of core orthologs and the selection of data subsets by matrix reduction can have marked effects on the reconstructed phylogenetic trees. Nonetheless, all eight data sets strongly support Pancrustacea with Remipedia as the sister group to Hexapoda. This is the first time that a sister group relationship of Remipedia and Hexapoda has been inferred using a comprehensive phylogenomic data set that is based on EST data. We also show that selecting data subsets with increased overall signal can help to identify and prevent artifacts in phylogenetic analyses.
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              Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification.

              Caenorhabditis elegans is renowned for its invariant embryogenesis. This pattern of development is in apparent contrast to other organisms from Drosophila to higher vertebrates. With the aid of a 4D microscope system (multifocal, time-lapse video recording system) which permits the extensive documentation and analysis of cell divisions, cell positions, and migrations in single embryos we have analyzed normal embryogenesis of C. elegans. The instrumentation reveals a naturally occurring variability in cell division timing, cell positioning, and cell-cell contacts which could not have been detected by the direct observation used earlier (Sulston et al., 1983, Dev. Biol. 100, 64-119). Embryos are very flexible and produce an essentially invariant premorphogenetic stage from variable earlier stages. An analysis of the distribution of the descendants of the early founder blastomeres at the premorphogenetic stage shows that these establish discrete regions in the embryo, a process involving a considerable amount of cell movement, which again varies in different embryos. Only cell fate assignment remains invariant. However, as shown earlier, this is not due to an autonomous invariant specification of cell fates but due to the fact that cell-cell interactions occur very early when the topology of blastomeres in the embryo is still sufficiently precise to ensure reproducible patterns of inductions. A new concept that founder blastomeres produce embryonic regions in the embryo can explain the striking complexity of the lineage per se and also the complicated asymmetric lineage patterns by which the bilateral symmetry of the embryo is established. Many cells, including bilateral homologs, were apparently chosen for a specific fate solely by their position in the embryo, irrespectively of the lineage descent by which the cells are created. We postulate that the production of regions by cell-cell interactions is the pivotal principle guiding the embryogenesis of C. elegans and that the embryogenesis of the worm follows the same basic principles as embryogenesis in other organisms.
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                Author and article information

                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central
                1742-9994
                2014
                7 February 2014
                : 11
                : 10
                Affiliations
                [1 ]Humboldt-Universität zu Berlin, Institut für Biologie/Vergleichende Zoologie, Philippstr. 13, 10115 Berlin, Germany
                [2 ]Current address: Institut de Génomique Fonctionnelle de Lyon (IGFL), 32-34 avenue Tony Garnier, Lyon 69007, France
                Article
                1742-9994-11-10
                10.1186/1742-9994-11-10
                3930293
                24507018
                28becd5c-0c59-4b5b-b68b-e1dafbc750e4
                Copyright © 2014 Alwes and Scholtz; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 25 November 2013
                : 30 January 2014
                Categories
                Research

                Animal science & Zoology
                cladocera,crustacea,cell lineage,cleavage pattern,development
                Animal science & Zoology
                cladocera, crustacea, cell lineage, cleavage pattern, development

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