Sumario:
The International Journal of Developmental Biology
Linking Development, Stem Cells and Cancer Research
Euskal Herriko Unibertsitateko Argitalpen Zerbitzua / Servicio Editorial de la Universidad del País Vasco / University of the Basque Country Press
Volume 58 - Numbers 6-7-8 (2014) / Pages 385-643 Editor-in-Chief: Juan Aréchaga
MORE INFORMATION [Abstract - FullText / FullText Open Access]
ISSN: 0214-6282 / ISSN-e: 1696-3547 www.intjdevbiol.com
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Special Issue: Spiralian Model Systems
Guest Editor: Jonathan Henry
ABSTRACTS
Preface
Contemporary Spiralian Developmental Biology
Jonathan Henry ..... p. 385
Department of Cell & Developmental Biology, University of Illinois, Urbana, IL, USA
Abstract: This current issue of The International Journal of Developmental Biology focuses attention on many models that represent the metazoan super-clade called the Spiralia (Lophotrochozoa). This clade encompasses the largest number of metazoan phyla, with arguably the most diverse array of animal body plans.
Keywords: bilaterian metazoan, spiral cleavage, life history strategy
Introduction to Spiralian Model Systems
EHU/UPV/UBC - The International Journal of Developmental Biology 58: 389-401 (2014)
doi: 10.1387/ijdb.140127jh / © UBC Press (www.a360grados.net)
Spiralian model systems
Jonathan Q. Henry
Department of Cell & Developmental Biology, University of Illinois, Urbana, IL, USA
Abstract: The “Spiralia” represent one of the three major clades of bilaterian metazoans. Though members of this clade exhibit tremendous diversity in terms of their larval and adult body plans, many share a highly conserved early pattern of development involving a stereotypic cleavage program referred to as spiral cleavage. This group therefore represents an excellent one in which to undertake comparative studies to understand the origins of such diversity from a seemingly common ground plan. These organisms also present varied and diverse modes in terms of their ecology, development and life history strategies. A number of well established and emerging model systems have been developed to undertake studies at the molecular, genetic, cell and organismal levels. The Special Issue of the Int. J. Dev. Biol. entitled “Spiralian Model Systems” focuses on these organisms and here, I introduce this clade, pointing out different types of studies being undertaken with representative spiralian model systems.
Keywords: bilaterian metazoan, spiral cleavage, life history strategy
Embryonic Development -------------------------------------------
EHU/UPV/UBC - The International Journal of Developmental Biology 58: 403-411 (2014)
doi: 10.1387/ijdb.140125nr / © UBC Press (www.a360grados.net)
Establishing the germline in spiralian embyos
Nicole Rebscher
Morphology and Evolution of Invertebrates, Phillips Universität Marburg, Marburg, Germany
Abstract: Elucidating the origin of germ cells in embryos and larvae is often obscured by the fact that the typical germ cell markers vasa, nanos and piwi are not exclusively expressed in primordial germ cells (PGCs), but are also commonly found in undifferentiated somatic tissues and stem cells as part of an evolutionary conserved ‘germline multipotency program’ (Juliano et al., 2010). Hidden in the crowd of undifferentiated cells, the PGCs have occasionally been overlooked and their formation during early embryogenesis was only revealed recently by new methodological approaches (e.g. Wu et al., 2011). Spiralians are excellent model organisms to deepen our understanding of PGC formation, given the highly stereotypical cleavage that occurs during embryogenesis. In these species, detailed cell lineage studies enable the tracing of single cells up to gastrulation stages. Here, I review our knowledge of the origin of PGCs in these invertebrates. Similarities in PGC formation among spiralian phyla as well as peculiarities of the highly derived clitellates are discussed with respect to developmental mode and evolution. Furthermore, the issue of gonad regeneration in platyhelminths and the asexually reproducing oligochaete Enchytraeus japonensis is addressed. An alternative strategy of compensating for caudal regeneration is presented for the polychaete Platynereis dumerilli. Finally, the molecular bases of PGC specification and the question of germplasm are discussed.
Keywords: Spiralia, primordial germ cell, mesoblast, vasa, nanos, PIWI
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 413-428 (2014)
doi: 10.1387/ijdb.140151dl / © UBC Press (www.a360grados.net)
Ins and outs of Spiralian gastrulation
Deirdre C. Lyons, 1 and Jonathan Q. Henry, 2
1. Duke University, Biology Department, Durham, NC, USA
2. University of Illinois, Dept. Cell & Developmental Biology, Urbana, IL, USA
Abstract: Gastrulation is a critical stage of metazoan development during which endodermal and mesodermal tissues are internalized, and morphogenesis transforms the early embryo into each animal’s unique body-plan. While gastrulation has been studied extensively in classic model systems such as flies, worms, and vertebrates, less is known about gastrulation at a mechanistic level in other taxa. Surprisingly, one particularly neglected group constitutes a major branch of animals: the Spiralia. A unique feature of spiralian development is that taxa with diverse adult body-plans, such as annelids, molluscs, nemerteans and platyhelminths all share a highly stereotyped suite of characters during embryogenesis called spiral cleavage. The spiral cleavage program makes it possible to compare distantly related embryos using not only morphological features, and gene expression patterns, but also homologous cell lineages. Having all three criteria available for comparison is especially critical for understanding the evolution of a complex process like gastrulation. Thus studying gastrulation in spiralians is likely to lead to novel insights about the evolution of body-plans, and the evolution of morphogenesis itself. Here we review relevant literature about gastrulation in spiralians and frame questions for future studies. We describe the internalization of the endoderm, endomesoderm and ectomesoderm; where known, we review data on the cellular and molecular control of those processes. We also discuss several morphogenetic events that are tied to gastrulation including: axial elongation, origins of the mouth and anus, and the fate of the blastopore. Since spiral cleavage is ancestral for a major branch of bilaterians, understanding gastrulation in spiralians will contribute more broadly to ongoing debates about animal body-plan divergence, such as: the origin of the through-gut, the emergence of indirect versus direct development, and the evolution of gene-regulatory networks that specify endomesoderm. We emphasize the fact that spiralian gastrulation provides the unique opportunity to connect well-defined embryonic cell lineages to variation in cell fate and cell behavior, making it an exceptional case study for evo-devo.
Keywords: spiralia, endomesoderm, ectomesoderm, blastopore, axial elongation, epiboly, invagination
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 429-443 (2014)
doi: 10.1387/ijdb.140132dw / © UBC Press (www.a360grados.net)
Developmental biology of the leech Helobdella
David A. Weisblat 1 and Dian-Han Kuo 2
1. Dept. of Molecular and Cell Biology, University of California, Berkeley, USA
2. Dept. of Life Science, National Taiwan University, Taiwan.
Abstract: Glossiphoniid leeches of the genus Helobdella provide experimentally tractable models for studies in evolutionary developmental biology (Evo-Devo). Here, after a brief rationale, we will summarize our current understanding of Helobdella development and highlight the near term prospects for future investigations, with respect to the issues of: D quadrant specification; the transition from spiral to bilaterally symmetric cleavage; segmentation, and the connections between segmental and non-segmental tissues; modifications of BMP signaling in dorsoventral patterning and the O-P equivalence group; germ line specification and genome rearrangements. The goal of this contribution is to serve as a summary of, and guide to, published work.
Keywords: embryonic patterning, Helobdella, leech, Lophotrochozoa, spiralian
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 445-456 (2014)
doi: 10.1387/ijdb.140102ts / © UBC Press (www.a360grados.net)
Developmental significance of D quadrant micromeres 2d and 4d in the oligochaete annelid Tubifex tubifex
Takashi Shimizu 1 and Ayaki Nakamoto 2
1. Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo, Japan
2. Department of Molecular and Cellular Biology, University of Arizona, Tucson, USA
Abstract: The annelid Tubifex tubifex is a cosmopolitan freshwater oligochaete and a member of the Spiralia, a large group of invertebrate phyla displaying spiral development. Because its developing eggs are easily obtained in the laboratory, this animal has long been used as material for developmental studies, especially spiralian embryology. In spiralian embryos, it has long been known that one blastomere at the four-cell stage, the D cell, and its direct descendants play an important role in axial pattern formation. Various studies have suggested that the D quadrant functions as the organizer of the embryonic axes in molluscs and annelids, and it has recently been demonstrated that the D quadrant micromeres, 2d11 and 4d, which had been transplanted to an ectopic position in an otherwise intact embryo induce a secondary embryonic axis to give rise to the formation of duplicated heads and/or tails. That 2d and 4d play a pivotal role in Tubifex embryonic development was first suggested from the classic cell-ablation experiments carried out in the early 1920s, and this has been confirmed by the recent cell-ablation/restoration experiments using cell-labeling with lineage tracers. These studies have also shown that in the operated embryos, none of the remaining cells can replace the missing 2d and 4d and that both 2d and 4d are determined as ectodermal and mesodermal precursors, respectively, at the time of their birth. The anteroposterior polarity of these micromeres is also specified at the time of their birth, suggesting that nascent 2d and 4d are specified in their axial properties as well as in cell fate decision.
Keywords: D quadrant, 2d, 4d, cell lineage, embryonic axis, axial organizer, anteroposterior polarity, Tubifex tubifex
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 457-467 (2014)
doi: 10.1387/ijdb.140154es / © UBC Press (www.a360grados.net)
Variation in spiralian development: insights from polychaetes
Elaine C. Seaver
Whitney Laboratory for Marine Bioscience, University of Florida, FL, USA
Abstract: Spiralian development is characterized by the conservation of spindle orientation and cell geometry during early cleavage stages, as well as features of the ultimate fates of identified cells. This complex set of characters is shared by a number of animal lineages including nemerteans, polyclad platyhelminthes, annelids and mollusks. How a similar, highly stereotypical cleavage program can give rise to such diversity of larval and adult forms has intrigued researchers for many years. This review summarizes recent data from polychaete annelids, and highlights both conservation and variation in the cellular and molecular mechanisms that guide the spiral cleavage developmental program. There is a specific focus on comparisons of fate maps, patterns of cleavage, mechanisms of cell fate specification, organizing activity, and differences in molecular patterning. Some of the differences in early development represent intra-clade variation within annelids, and others hint at differences between annelids and other taxa. Because much of the classic work on spiralians has focused on mollusks, these new data from annelids have expanded our knowledge about the evolutionary flexibility in spiralian development and potentially its role in body plan evolution.
Keywords: spiralian, polychaete, fate specification
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 469-483 (2014)
doi: 10.1387/ijdb.140148gb / © UBC Press (www.a360grados.net)
Segment formation in Annelids: patterns, processes and evolution
Guillaume Balavoine
Institut Jacques Monod, CNRS / Université Paris Diderot, Paris, France
Abstract: The debate on the origin of segmentation is a central question in the study of body plan evolution in metazoans. Annelids are the most conspicuously metameric animals as most of the trunk is formed of identical anatomical units. In this paper, I summarize the various patterns of evolution of the metameric body plan in annelids, showing the remarkable evolvability of this trait, similar to what is also found in arthropods. I then review the different modes of segment formation in the annelid tree, taking into account the various processes taking place in the life histories of these animals, including embryogenesis, post-embryonic development, regeneration and asexual reproduction. As an example of the variations that occur at the cellular and genetic level in annelid segment formation, I discuss the processes of teloblastic growth or posterior addition in key groups in the annelid tree. I propose a comprehensive definition for the teloblasts, stem cells that are responsible for sequential segment addition. There are a diversity of different mechanisms used in annelids to produce segments depending on the species, the developmental time and also the life history processes of the worm. A major goal for the future will be to reconstitute an ancestral process (or several ancestral processes) in the ancestor of the whole clade. This in turn will provide key insights in the current debate on ancestral bilaterian segmentation.
Keywords: segmentation, metamerism, annelid, evolution, teloblasts
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 485-499 (2014)
doi: 10.1387/ijdb.140095mb / © UBC Press (www.a360grados.net)
Sipuncula: an emerging model of spiralian development and evolution
Michael J. Boyle 1and Mary E. Rice 2
1. Smithsonian Tropical Research Institute (STRI), Panama, Republic of Panama
2. Smithsonian Marine Station at Fort Pierce (SMSFP), Florida, USA
Abstract: Sipuncula is an ancient clade of unsegmented marine worms that develop through a conserved pattern of unequal quartet spiral cleavage. They exhibit putative character modifications, including conspicuously large first-quartet micromeres and prototroch cells, postoral metatroch with exclusive locomotory function, paired retractor muscles and terminal organ system, and a U-shaped digestive architecture with left-right asymmetric development. Four developmental life history patterns are recognized, and they have evolved a unique metazoan larval type, the pelagosphera. When compared with other quartet spiral-cleaving models, sipunculan development is understudied, challenging and typically absent from evolutionary interpretations of spiralian larval and adult body plan diversity. If spiral cleavage is appropriately viewed as a flexible character complex, then understudied clades and characters should be investigated. We are pursuing sipunculan models for modern molecular, genetic and cellular research on evolution of spiralian development. Protocols for whole mount gene expression studies are established in four species. Molecular labeling and confocal imaging techniques are operative from embryogenesis through larval development. Next-generation sequencing of developmental transcriptomes has been completed for two species with highly contrasting life history patterns, Phascolion cryptum (direct development) and Nephasoma pellucidum (indirect planktotrophy). Looking forward, we will attempt intracellular lineage tracing and fate-mapping studies in a proposed model sipunculan, Themiste lageniformis. Importantly, with the unsegmented Sipuncula now repositioned within the segmented Annelida, sipunculan worms have become timely and appropriate models for investigating the potential for flexibility in spiralian development, including segmentation. We briefly review previous studies, and discuss new observations on the spiralian character complex within Sipuncula.
Keywords: pelagosphera, metatroch, unequal, U-shaped, ectomesoderm
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 501-511 (2014)
doi: 10.1387/ijdb.140121ad / © UBC Press (www.a360grados.net)
A conserved set of maternal genes? Insights from a molluscan transcriptome
M. Maureen Liu 1,2, John W. Davey 3,4, Daniel J. Jackson 5, Mark L. Blaxter 3,6 and Angus Davison 1
1. School of Life Sciences, University of Nottingham, University Park, Nottingham, UK
2. Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, UK
3. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK
4. Department of Zoology, University of Cambridge, Downing Street, Cambridge, UK
5. Courant Research Centre for Geobiology, University of Göttingen, Göttingen, Germany
6. Edinburgh Genomics, School of Biological Sciences, University of Edinburgh, Edinburgh, UK
Abstract: The early animal embryo is entirely reliant on maternal gene products for a ‘jump-start’ that transforms a transcriptionally inactive embryo into a fully functioning zygote. Despite extensive work on model species, it has not been possible to perform a comprehensive comparison of maternally-provisioned transcripts across the Bilateria because of the absence of a suitable dataset from the Lophotrochozoa. As part of an ongoing effort to identify the maternal gene that determines left-right asymmetry in snails, we have generated transcriptome data from 1 to 2-cell and ~32-cell pond snail (Lymnaea stagnalis) embryos. Here, we compare these data to maternal transcript datasets from other bilaterian metazoan groups, including representatives of the Ecydysozoa and Deuterostomia. We found that between 5 and 10% of all L. stagnalis maternal transcripts (~300-400 genes) are also present in the equivalent arthropod (Drosophila melanogaster), nematode (Caenorhabditis elegans), urochordate (Ciona intestinalis) and chordate (Homo sapiens, Mus musculus, Danio rerio) datasets. While the majority of these conserved maternal transcripts (“COMATs”) have housekeeping gene functions, they are a non-random subset of all housekeeping genes, with an overrepresentation of functions associated with nucleotide binding, protein degradation and activities associated with the cell cycle. We conclude that a conserved set of maternal transcripts and their associated functions may be a necessary starting point of early development in the Bilateria. For the wider community interested in discovering conservation of gene expression in early bilaterian development, the list of putative COMATs may be useful resource.
Keywords: maternal to zygotic transition, mollusk, MBT, MZT, Spiralia
Molecular Level Control of Development --------------------------------------
EHU/UPV/UBC - The International Journal of Developmental Biology 58: 513-520 (2014)
doi: 10.1387/ijdb.140087rk / © UBC Press (www.a360grados.net)
Spiral cleavages determine the left-right body plan by regulating Nodal pathway in monomorphic gastropods, Physa acuta
Masanori Abe, Hiromi Takahashi and Reiko Kuroda
Research Institute for Science and Technology, Tokyo University of Science, Yamazaki, Noda-shi, Chiba, Japan
Abstract: The handedness of gastropods is genetically determined, but the molecular nature of the gene responsible and the associated mechanisms remain unknown. In order to characterize the chiromorphogenesis pathway starting from the gene to the left-right asymmetric body plan, we have closely analyzed the cytoskeletal dynamics of the Physa (P.) acuta embryo, a fresh water non-dimorphic sinistral snail, during the early developmental stage by mechanically altering the handedness of the embryos at the critical spiral third cleavage. A fertile situs inversus was created and the nodal-Pitx gene expression patterns were completely mirror imaged to the wild type at the trochophore stage. Together with our previous work on Lymnaea (L.) stagnalis, we could show that chirality is established at the third cleavage, as dictated by the single handedness-determining gene locus, and then chirality information is transferred via subsequent spiral fourth and fifth cleavages to the later developmental stage, dictating the nodal-Pitx expression pathway. The cytoskeletal dynamics of manipulated and non-manipulated embryos of sinistral P. acuta and dextral dominant L. stagnalis are compared.
Keywords: spiral cleavage, nodal pathway, chirality, shell coiling, gastropod
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 521-532 (2014)
doi: 10.1387/ijdb.140133cg / © UBC Press (www.a360grados.net)
Evolution, divergence and loss of the Nodal signalling pathway: new data and a synthesis across the Bilateria
Cristina Grande 1, José María Martín-Durán 2 Nathan J. Kenny 3, Marta Truchado-García 1 and Andreas Hejnol 2
1. Departamento de Biología Molecular and Centro de Biología Molecular "Severo Ochoa" (Consejo Superior de Investigaciones Científicas - Universidad Autónoma de Madrid), Madrid, Spain
2. Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen, Norway
3. Evolution and Development Research Group, Department of Zoology, University of Oxford, UK
Abstract: Since the discovery that the TGF-? signalling molecule Nodal and its downstream effector Pitx have a parallel role in establishing asymmetry between molluscs and deuterostomes the debate over the degree to which this signalling pathway is conserved across the Bilateria as a whole has been ongoing. Further taxon sampling is critical to understand the evolution and divergence of this signalling pathway in animals. Using genome and transcriptome mining we confirmed the presence of nodal and Pitx in a range of additional animal taxa for which their presence has not yet been described. In situ hybridization was used to show the embryonic expression of these genes in brachiopods and planarians. We show that both nodal and Pitx genes are broadly conserved across the Spiralia, and nodal likely appeared in the Bilaterian stem lineage after the divergence of the Acoelomorpha. Furthermore, both nodal and Pitx mRNA appears to be expressed in an asymmetric fashion in the brachiopod Terebratalia transversa. No evidence for the presence of a Lefty ortholog could be found in the non-deuterostome genomic resources examined. Nodal expression is asymmetric in a number of spiralian lineages, indicating a possible ancestral role of the Nodal/Pitx cascade in the establishment of asymmetries across the Bilateria.
Keywords: Nodal, Pitx, Spiralia, Bilateria, Brachiopoda
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 533-549 (2014)
doi: 10.1387/ijdb.140080nk / © UBC Press (www.a360grados.net)
The Lophotrochozoan TGF-β signalling cassette - diversification and conservation in a key signalling pathway
Nathan J. Kenny 1,3, Erica K.O. Namigai 1, Peter K. Dearden 2, Jerome H.L. Hui 3, Cristina Grande 4 and Sebastian M. Shimeld 1
1. Evolution and Development Research Group, Department of Zoology, University of Oxford, UK
2. Laboratory for Evolution and Development, Genetics Otago and Gravida, The National Centre for Growth and Development, Biochemistry Department, University of Otago, Aotearoa, New Zealand
3. School of Life Sciences, Chinese University of Hong Kong, Shatin, Hong Kong
4. Departamento de Biología Molecular and Centro de Biología Molecular "Severo Ochoa", CSIC-Universidad Autónoma de Madrid, Madrid, Spain
Abstract: TGF-β signalling plays a key role in the patterning of metazoan body plans and growth. It is widely regarded as a ‘module’ capable of co-option into novel functions. The TGF-β pathway arose in the Metazoan lineage, and while it is generally regarded as well conserved across evolutionary time, its components have been largely studied in the Ecdysozoa and Deuterostomia. The recent discovery of the Nodal molecule in molluscs has underlined the necessity of untangling this signalling network in lophotrochozoans in order to truly comprehend the evolution, conservation and diversification of this key pathway. Three novel genome resources, the mollusc Patella vulgata, annelid Pomatoceros lamarcki and rotifer Brachionus plicatilis, along with other publicly available data, were searched for the presence of TGF-β pathway genes. Bayesian and Maximum Likelihood analyses, along with some consideration of conserved domain structure, was used to confirm gene identity. Analysis revealed conservation of key components within the canonical pathway, allied with extensive diversification of TGF-β ligands and partial loss of genes encoding pathway inhibitors in some lophotrochozoan lineages. We fully describe the TGF-β signalling cassette of a range of lophotrochozoans, allowing firm inference to be drawn as to the ancestral state of this pathway in this Superphylum. The TGF-β signalling cascade’s reputation as being highly conserved across the Metazoa is reinforced. Diversification within the activin-like complement, as well as potential wide loss of regulatory steps in some Phyla, hint at specific evolutionary implications for aspects of this cascade’s functionality in this Superphylum.
Keywords: TGF-β, Lophotrochozoa, BMP, Activin, signalling
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 551-562 (2014)
doi: 10.1387/ijdb.140149ln / © UBC Press (www.a360grados.net)
Ilyanassa Notch signaling implicated in dynamic signaling between all three germ layers
Maey Gharbiah 1, Ayaki Nakamoto 1, Adam B. Johnson 2, J. David Lambert 2 and Lisa M. Nagy 1
1. Department of Molecular and Cellular Biology, University of Arizona, Tucson, Arizona, USA
2. Department of Biology, University of Rochester, NY, USA
Abstract: Two cells (3D and 4d) in the mud snail Ilyanassa obsoleta function to induce proper cell fate. In this study, we provide support for the hypothesis that Notch signaling in Ilyanassa obsoleta functions in inductive signaling at multiple developmental stages. The expression patterns of Notch, Delta and Suppressor of Hairless (SuH) are consistent with a function for Notch signaling in endoderm formation, the function of 3D/4d and the sublineages of 4d. Veligers treated with DAPT show a range of defects that include a loss of endodermal structures, and varying degrees of loss of targets of 4d inductive signaling. Veligers that result from injection of Ilyanassa Delta siRNAi in general mimic the defects observed in the DAPT treated larvae. The most severe DAPT phenotypes mimic early ablations of 4d. However, the early specification of 4d itself appears normal and MAPK activation in both 3D/4d and the micromeres, which are known to activate MAPK as a result of 3D/4d induction, are normal in DAPT treated larvae. Treating larvae at successively later timepoints with DAPT suggests that Notch/Delta signaling is not only required during early 4d inductive signaling, but during subsequent stages of cell fate determination as well. Based on our results, combined with previous reports implicating the endoderm in maintaining induced fate specification in Ilyanassa, we propose a speculative model that Notch signaling is required to specify endoderm fates and 4d sublineages, as well as to maintain cell fates induced by 4d.
Keywords: Notch, Delta, mollusc, endoderm, 4d
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 563-573 (2014)
doi: 10.1387/ijdb.140084ss / © UBC Press (www.a360grados.net)
Expression of the wnt gene complement in a spiral-cleaving embryo and trochophore larva
Margaret M. Pruitt, Edward J. Letcher, Hsien-Chao Chou, Benjamin R. Bastin and Stephan Q. Schneider
Department of Genetics, Development and Cell Biology, Iowa State University, Ames, IA, USA
Abstract: The highly conserved wnt gene family has roles in developmental processes ranging from axis formation to cell fate determination. The polychaete Platynereis dumerilii has retained 12 of the 13 ancient wnt subfamilies and is a good model system to study the roles of the wnt ligands in spiralian development. While it has been shown that Platynereis uses a global beta-catenin-mediated binary cell fate specification module in development, the early roles of the 12 wnt genes present in Platynereis are unknown. Transcriptional profiling by RNA-Seq during early development and whole-mount in situ hybridization of embryo and larval stages were used to determine the temporal and spatial regulation of the wnt complement in Platynereis. None of the 12 wnt transcripts were maternally provided at significant levels. In pregastrula embryos, zygotic wntA, wnt4, and wnt5 transcripts exhibited distinctive patterns of differential gene expression. In contrast, in trochophore larvae, all 12 wnt ligands were expressed and each had a distinct expression pattern. While three wnt ligands were expressed in early development, none were expressed in the right place for a widespread role in beta-catenin-mediated binary specification in early Platynereis development. However, the expression patterns of the wnt ligands suggest the presence of numerous wnt signaling centers, with the most prominent being a bias for staggered posterior wnt expression in trochophore larvae. The similarity to wnt expression domains in cnidarians around the blastopore and the tail organizer in chordates supports a hypothesis of a common evolutionary origin of posterior organizing centers.
Keywords: wnt, spiral cleaving, signaling center, trochophore, polychaete
Life History Strategies -------------------------------------------------
EHU/UPV/UBC - The International Journal of Developmental Biology 58: 575-583 (2014)
doi: 10.1387/ijdb.140100ca / © UBC Press (www.a360grados.net)
Development of a feeding trochophore in the polychaete Hydroides elegans
Cesar Arenas-Mena 1 and Ava Li 2
1. Department of Biology, College of Staten Island and Graduate Center, The City University of New York (CUNY), NY
2. Broad Institute of MIT, MA, USA
Abstract: Hydroides elegans is an indirectly developing polychaete with equal spiral cleavage, gastrulation by invagination, and a feeding trochophore. Expression of several transcription factors and differentiation genes has been characterized. Comparative analysis reveals evolutionarily conserved roles. For example, the synexpression of transcription factors FoxA and Brachyury suggests homology of primary and secondary gut openings in protostomes and deuterostomes, and the expression of Sall suggests similar regulatory controls in the posterior growth zone of bilaterians. Differences in gene expression suggest regulatory differences control gastrulation by invagination in polychaetes with a feeding trochophore and gastrulation by epiboly in polychaetes without a feeding trochophore. Association of histone variant H2A.Z with transcriptional potency and its expression suggest a developmental role during both embryogenesis and the larva-to-adult transformation. Methods are being developed for experimental exploration of the gene regulatory networks involved in trochophore development in Hydroides. It is unknown if polychaete feeding trochophores evolved from a larval stage already present in the life cycle of the last common ancestor of protostomes and deuterostomes. Previous evolutionary scenarios about larval origins overemphasize the discontinuity between larval and adult development and require the early evolution of undifferentiated and transcriptionally potent “set aside” cells. Indirect development may proceed by developmental remodeling of differentiated cells and could have evolved after gradual transformation of juveniles into larvae; undifferentiated and transcriptionally potent cells would have evolved secondarily. Comprehensive characterization of gene regulatory networks for feeding trochophore development may help resolve these major evolutionary questions.
Keywords: bilaterian, posterior growth, serpulid, annelid
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 585-591 (2014)
doi: 10.1387/ijdb.140090sm / © UBC Press (www.a360grados.net)
From trochophore to pilidium and back again - a larva’s journey
Svetlana A. Maslakova* and Terra C. Hiebert
Oregon Institute of Marine Biology, University of Oregon, OR, USA
Abstract: Nemerteans, a phylum of marine lophotrochozoan worms, have a biphasic life history with benthic adults and planktonic larvae. Nemertean larval development is traditionally categorized into direct and indirect. Indirect development via a long-lived planktotrophic pilidium larva is thought to have evolved in one clade of nemerteans, the Pilidiophora, from an ancestor with a uniformly ciliated planuliform larva. Planuliform larvae in a member of a basal nemertean group, the Palaeonemertea, have been previously shown to possess a vestigial prototroch, homologous to the primary larval ciliated band in the trochophores of other spiralian phyla, such as annelids and mollusks. We review literature on nemertean larval development, and include our own unpublished observations. We highlight recent discoveries of numerous pilidiophoran species with lecithotrophic larvae. Some of these larvae superficially resemble uniformly ciliated planuliform larvae of other nemerteans. Others possess one or two transverse ciliary bands, which superficially resemble the prototroch and telotroch of some spiralian trochophores. We also summarize accumulating evidence for planktotrophic feeding by larvae of the order Hoplonemertea, which until now were considered to be lecithotrophic. We suggest that 1) non-feeding pilidiophoran larval forms are derived from a feeding pilidium; 2) such forms have likely evolved many times independently within the Pilidiophora; 3) any resemblance of such larvae to the trochophores of other spiralians is a result of convergence and that 4) the possibility of planktotrophy in hoplonemertean larvae may influence estimates of pelagic larval duration, dispersal, and population connectivity in this group.
Keywords: nemertea, larval development, lecithotrophy, planktotrophy
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 593-599 (2014)
doi: 10.1387/ijdb.140088mr / © UBC Press (www.a360grados.net)
Dimorphic development in Streblospio benedicti: genetic analysis of morphological differences between larval types
Christina Zakas and Matthew V. Rockman
Department of Biology and Center for Genomics & Systems Biology, New York University, New York, NY, USA
Abstract: The marine polychaete Streblospio benedicti exhibits two distinct larval types, making it a model for the study of developmental evolution. Females produce either large eggs or small ones, which develop into distinct lecithotrophic or planktotrophic larvae with concomitant morphological and life-history differences. Here, we investigate the inheritance of key morphological traits that distinguish the larval types. We used genetic crosses to establish the influence of maternal and zygotic differences on larval phenotypes. We found a large maternal effect on larval size and the number of larval chaetae, while the number and length of these chaetae were also strongly influenced by zygotic genotype. Interestingly, the distribution of larval phenotypes produced by these crosses suggests traits intermediate to the two parental types should not be uncommon. Yet, despite gene flow between the types in natural populations, such intermediates are rarely found in nature, suggesting that selection may be maintaining distinct larval modes.
Keywords: Streblospio benedicti, poecilogony, quantitative genetics, life-history evolution
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 601-611 (2014)
doi: 10.1387/ijdb.140136rc / © UBC Press (www.a360grados.net)
The development of viable and nutritive embryos in the direct developing gastropod Crepidula navicella
Maryna P. Lesoway 1,2, Ehab Abouheif 1 and Rachel Collin 2
1. McGill University, Montreal, QC, Canada
2. Smithsonian Tropical Research Institute, Balboa, Ancon, Republic of Panama
Abstract: Adelphophagy occurs when encapsulated embryos complete development by feeding on their developing siblings, which are known as nutritive embryos. Nutritive embryos are found in a variety of animal groups, and are especially common in some groups of marine invertebrates. Although they have evolved numerous times independently in the calyptraeid gastropods, adelphophagic development with nutritive embryos has not been described in detail. Using light microscopy and time-lapse imaging of laboratory-reared embryos, we describe the development of Crepidula navicella, a direct developer with nutritive embryos that cleave and gastrulate. Early stages of nutritive and viable embryos do not show any obvious morphological differences, but do show asynchrony in early cleavage among embryos from the same capsule. We discovered that two classes of nutritive embryos are produced; gastrula-like nutritive embryos, which arrest after gastrulation, and post-gastrula-like nutritive embryos that are more variable in morphology, and show evidence of minor differentiation. This study provides a framework for future research on the developmental and molecular mechanisms of nutritive embryo development of C. navicella, which will allow us to address the role of nutritive embryos in the origins of developmental polyphenisms. Careful description of the developmental sequence is necessary before adaptive hypotheses can be addressed, and comparisons with other taxa can be made. Understanding the different ways that embryos and their development are disrupted to produce nutritive embryos will provide important insights into the normal process of development.
Keywords: developmental timeline, adelphophagy, nutritive embryos, nurse eggs, trophic eggs
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 613-622 (2014)
doi: 10.1387/ijdb.140081cb / © UBC Press (www.a360grados.net)
An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)
Conrad Helm 1, Helge Adamo 1, Stephane Hourdez 2,3, Christoph Bleidorn 1
1. Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig, Leipzig, Germany
2. CNRS, Equipe ABICE, UMR7144, Station Biologique de Roscoff
3. UPMC Université Paris 06, Equipe ABICE, UMR7144, Station Biologique de Roscoff, Roscoff, France
Abstract: The nereidid annelid Platynereis dumerilii emerged as a well-understood model organism. P. dumerilii and P. massiliensis are sister taxa, which are morphologically indistinguishable as adults. Interestingly, they exhibit highly contrasting life-histories: while P. dumerilii is a gonochorostic species with planktonic feeding larvae, P. massiliensis is a protandric hermaphrodite with lecitotrophic semi-direct -development in brood tubes. Using light microscopy and immunohistochemical methods coupled with confocal laser scanning microscopy, we describe the development of P. massiliensis. Musculature was stained with phalloidin-rhodamine. FMRFamide, acetylated ?-tubulin, and serotonin were targeted by antibodies for the staining of neuronal structures. Additionally, eye development was investigated with the specific 22C10-antibody. The development of P. massiliensis is characterized by the absence of a free-swimming stage, a late development of food uptake, and the presence of a large amount of yolk even in late juvenile stages. Most notably, early juvenile stages already exhibit an organization of several organ systems that resembles those of adults. Larval characters present in the free-swimming feeding larvae of P. dumerilii, as e.g. the apical organ and larval eyes, are absent and regarded to be lost in developing stages of P. massiliensis. Many of the differences found in the development of these two species can be described in the context of heterochronic changes. We strongly advocate expanding evolutionary developmental studies from the well-established model annelid P. dumerilii to the closely related P. massiliensis to study the evolutionary conservation and divergence of genetic pathways involved in developmental processes.
Keywords: cLSM, evodevo, eye development, heterochrony, model organism, polychaete
Regenerative Biology ---------------------------------------------------
EHU/UPV/UBC - The International Journal of Developmental Biology 58: 623-634 (2014)
doi: 10.1387/ijdb.140142ab / © UBC Press (www.a360grados.net)
Regeneration in spiralians: evolutionary patterns and developmental processes
Alexandra E. Bely 1, Eduardo E. Zattara 1,2 and James M. Sikes 3
1. Department of Biology, University of Maryland, College Park, Maryland, USA
2. Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington DC, USA
3. Department of Biology, University of San Francisco, San Francisco, California, USA
Abstract: Animals differ markedly in their ability to regenerate, yet still little is known about how regeneration evolves. In recent years, important advances have been made in our understanding of animal phylogeny and these provide new insights into the phylogenetic distribution of regeneration. The developmental basis of regeneration is also being investigated in an increasing number of groups, allowing commonalities and differences across groups to become evident. Here, we focus on regeneration in the Spiralia, a group that includes several champions of animal regeneration, as well as many groups with more limited abilities. We review the phylogenetic distribution and developmental processes of regeneration in four major spiralian groups: annelids, nemerteans, platyhelminths, and molluscs. Although comparative data are still limited, this review highlights phylogenetic and developmental patterns that are emerging regarding regeneration in spiralians and identifies important avenues for future research.
Keywords: regeneration, Annelida, Nemertea, Platyhelminthes, Mollusca
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EHU/UPV/UBC - The International Journal of Developmental Biology 58: 635-642 (2014)
doi: 10.1387/ijdb.140116df / © UBC Press (www.a360grados.net)
The dynamics of alkaline phosphatase activity during operculum regeneration in the polychaete Pomatoceros lamarckii
Réka Szabó and David E.K. Ferrier
The Scottish Oceans Institute, Gatty Marine Laboratory, University of St Andrews, Fife, UK
Abstract: Alkaline phosphatase enzymes are found throughout the living world and fulfil a variety of functions. They have been linked to regeneration, stem cells and biomineralisation in a range of animals. Here we describe the pattern of alkaline phosphatase activity in a spiralian appendage, the operculum of the serpulid polychaete Pomatoceros lamarckii. The P. lamarckii operculum is reinforced by a calcified opercular plate and is capable of rapid regeneration, making it an ideal model system to study these key processes in annelids. Alkaline phosphatase activity is present in mesodermal tissues of both intact and regenerating opercular filaments, in a strongly regionalised pattern correlated with major morphological features. Based on the lack of epidermal activity and the broad distribution of staining in mesodermal tissues, calcification- or stem cell-specific roles are unlikely. Transcriptomic data reveal that at least four distinct genes contribute to the detected activity. Opercular alkaline phosphatase activity is sensitive to levamisole. Phylogenetic analysis of metazoan alkaline phosphatases indicates homology of the P. lamarckii sequences to other annelid alkaline phosphatases, and shows that metazoan alkaline phosphatase evolution was characterised by extensive lineage-specific duplications.
Keywords: serpulid, calcification, biomineralisation, appendage regeneration
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