Morphological evolution and embryonic developmental diversity in metazoa

Most studies of pattern formation and morphogenesis in metazoans focus on a small number of model species, despite the fact that information about a wide range of species and developmental stages has accumulated in recent years. By contrast, this article attempts to use this broad knowledge base to arrive at a classification of developmental types through which metazoan body plans are generated. This classification scheme pays particular attention to the diverse ways by which cell signalling and morphogenetic movements depend on each other, and leads to several testable hypotheses regarding morphological variation within and between species, as well as metazoan evolution.

[1]  Matthew J. Hayden Embryology: Constructing the Organism , 2001, The Yale Journal of Biology and Medicine.

[2]  M. Shankland,et al.  Axial patterning in the leech: developmental mechanisms and evolutionary implications. , 1998, The Biological bulletin.

[3]  T. Mikawa,et al.  Induction and patterning of the primitive streak, an organizing center of gastrulation in the amniote , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  Stuart A. Newman,et al.  Problems and paradigms: Is segmentation generic? , 1993 .

[5]  Lesilee S. Rose,et al.  Asymmetric cell division and axis formation in the embryo. , 2005, WormBook : the online review of C. elegans biology.

[6]  C. Nielsen Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion. , 2005, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[7]  M. Wake,et al.  Quantitative Tests of General Models for the Evolution of Development , 2004, The American Naturalist.

[8]  R. Lanfear,et al.  Ancestral Notch-mediated segmentation revealed in the cockroach Periplaneta americana , 2008, Proceedings of the National Academy of Sciences.

[9]  L. Wolpert Developmental Biology , 1968, Nature.

[10]  R. Solé,et al.  Gene networks capable of pattern formation: from induction to reaction-diffusion. , 2000, Journal of theoretical biology.

[11]  Ariel D. Chipman,et al.  Arthropod Segmentation: beyond the Drosophila paradigm , 2005, Nature Reviews Genetics.

[12]  D. Loebel,et al.  Gene function in mouse embryogenesis: get set for gastrulation , 2007, Nature Reviews Genetics.

[13]  Ralph I. Smith,et al.  Embryology and Phylogeny in Annelids and Arthropods , 1974 .

[14]  J. Lemaire Table de developpement embryonnaire de Sepia officinalis L. (mollusque cephalopode) , 1970 .

[15]  S. Xiao,et al.  On the eve of animal radiation: phylogeny, ecology and evolution of the Ediacara biota. , 2009, Trends in ecology & evolution.

[16]  J T Bonner,et al.  PERSPECTIVE: THE SIZE‐COMPLEXITY RULE , 2004, Evolution; international journal of organic evolution.

[17]  S. Gould The Shape of Life , 1996 .

[18]  E. Davidson Spatial mechanisms of gene regulation in metazoan embryos. , 1991, Development.

[19]  W. W. Ballard Morphogenetic Movements and Fate Maps of Vertebrates , 1981 .

[20]  E. M. Del Pino,et al.  The pattern of early cleavage of the marsupial frog Gastrotheca riobambae. , 1990, Development.

[21]  Ray Keller,et al.  How we are shaped: the biomechanics of gastrulation. , 2003, Differentiation; research in biological diversity.

[22]  N. Gostling,et al.  From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design , 2002, Heredity.

[23]  B. Bowerman,et al.  Cell polarity in the early Caenorhabditis elegans embryo. , 1999, Current opinion in genetics & development.

[24]  G. Forgacs,et al.  Biological Physics of the Developing Embryo , 2005 .

[25]  Isaac Salazar-Ciudad,et al.  Tooth morphogenesis in vivo, in vitro, and in silico. , 2008, Current topics in developmental biology.

[26]  Xin Yi Chan,et al.  Widespread RNA segregation in a spiralian embryo , 2007, Evolution & development.

[27]  J Hardin,et al.  Getting into shape: epidermal morphogenesis in Caenorhabditis elegans embryos , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[28]  C. Heisenberg,et al.  Back and forth between cell fate specification and movement during vertebrate gastrulation. , 2008, Current opinion in genetics & development.

[29]  S. Newman Is segmentation generic? , 1993, BioEssays : news and reviews in molecular, cellular and developmental biology.

[30]  S. Morris The origins and relationships of lower invertebrates , 1983 .

[31]  E. Schierenberg Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications , 2005, Development Genes and Evolution.

[32]  M. Schoppmeier,et al.  Suppressor of Hairless and Presenilin phenotypes imply involvement of canonical Notch-signalling in segmentation of the spider Cupiennius salei. , 2005, Developmental biology.

[33]  Isaac Salazar-Ciudad,et al.  How different types of pattern formation mechanisms affect the evolution of form and development , 2004, Evolution & development.

[34]  S. Adamowicz,et al.  Increasing morphological complexity in multiple parallel lineages of the Crustacea , 2008, Proceedings of the National Academy of Sciences.

[35]  N. Papalopulu,et al.  Temporal and spatial expression of FGF ligands and receptors during Xenopus development , 2009, Developmental dynamics : an official publication of the American Association of Anatomists.

[36]  G. Wray The evolution of embryonic patterning mechanisms in animals. , 2000, Seminars in cell & developmental biology.

[37]  Michael Akam,et al.  The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair-rule gene homologues. , 2008, Developmental biology.

[38]  L. V. Belousov,et al.  The Dynamic Architecture of a Developing Organism: An Interdisciplinary Approach to the Development of Organisms , 1998 .

[39]  T. Williams,et al.  Developmental modularity and the evolutionary diversification of arthropod limbs. , 2001, The Journal of experimental zoology.

[40]  L. Salvini-Plawen On the origin and evolution of the lower Metazoa , 2009 .

[41]  D. Weisblat Asymmetric cell divisions in the early embryo of the leech Helobdella robusta. , 2007, Progress in molecular and subcellular biology.

[42]  B. Swalla,et al.  Nodal signaling and the evolution of deuterostome gastrulation , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  J. M. W. Slack,et al.  The zootype and the phylotypic stage , 1993, Nature.

[44]  H. Meinhardt Models for positional signalling with application to the dorsoventral patterning of insects and segregation into different cell types. , 1989, Development.

[45]  E. Schierenberg,et al.  Embryological variation during nematode development. , 2006, WormBook : the online review of C. elegans biology.

[46]  C. Heisenberg,et al.  Zebrafish gastrulation: cell movements, signals, and mechanisms. , 2007, International review of cytology.

[47]  M. Martindale,et al.  Unexpected complexity of the Wnt gene family in a sea anemone , 2005, Nature.

[48]  R. Keller,et al.  Morphogenic machines evolve more rapidly than the signals that pattern them: lessons from amphibians. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[49]  Y. Dong,et al.  Systematic functional analysis of the Caenorhabditis elegans genome using RNAi , 2003, Nature.

[50]  H. Nishida,et al.  Ascidian embryonic development: An emerging model system for the study of cell fate specification in chordates , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[51]  R. Raff The Shape of Life , 1996 .

[52]  H. Nishida Specification of embryonic axis and mosaic development in ascidians , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[53]  T. Fujisawa,et al.  Polyps, peptides and patterning , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[54]  M. Mercola,et al.  Distribution and functions of platelet-derived growth factors and their receptors during embryogenesis. , 1997, International review of cytology.

[55]  H. Nishida,et al.  Localized PEM mRNA and Protein Are Involved in Cleavage-Plane Orientation and Unequal Cell Divisions in Ascidians , 2007, Current Biology.

[56]  J. Finnerty,et al.  Origins of Bilateral Symmetry: Hox and Dpp Expression in a Sea Anemone , 2004, Science.

[57]  Arne Ø. Mooers,et al.  Size and complexity among multicellular organisms , 1997 .

[58]  M. Kai,et al.  Noncanonical Wnt/PCP signaling during vertebrate gastrulation. , 2009, Zebrafish.

[59]  Jeff Hardin,et al.  Epidermal morphogenesis. , 2005, WormBook : the online review of C. elegans biology.

[60]  M. Martindale,et al.  FGF signaling in gastrulation and neural development in Nematostella vectensis, an anthozoan cnidarian , 2007, Development Genes and Evolution.

[61]  A. Minelli,et al.  Conserved versus innovative features in animal body organization. , 2005, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[62]  Ekat Kritikou,et al.  Cell signalling: Divided divisions , 2005, Nature Reviews Molecular Cell Biology.

[63]  A. McGregor,et al.  Dynamic gene expression is required for anterior regionalization in a spider , 2009, Proceedings of the National Academy of Sciences.

[64]  M. Martindale,et al.  Cephalopod Hox genes and the origin of morphological novelties , 2003, Nature.

[65]  G. Scholtz,et al.  Cell lineage and cell fate in crustacean embryos--a comparative approach. , 1996, The International journal of developmental biology.

[66]  Susan J. Brown,et al.  A pair-rule gene circuit defines segments sequentially in the short-germ insect Tribolium castaneum. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[67]  J. Gibert,et al.  The evolution of engrailed genes after duplication and speciation events , 2002, Development Genes and Evolution.

[68]  R. Elinson,et al.  A novel development pattern for frogs: gastrulation produces an embryonic disk , 1983, Nature.

[69]  M. Richardson,et al.  Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  E. M. Pino Modifications of oogenesis and development in marsupial frogs , 1989 .

[71]  S. Roth,et al.  Dorsoventral Axis Formation in the Drosophila Embryo—Shaping and Transducing a Morphogen Gradient , 2005, Current Biology.

[72]  Sudhir Kumar,et al.  Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. , 2003, Molecular biology and evolution.

[73]  Susan J. Brown,et al.  Genetic regulation of engrailed and wingless in Tribolium segmentation and the evolution of pair-rule segmentation. , 2009, Developmental biology.

[74]  T. Holstein,et al.  Asymmetric expression of the BMP antagonists chordin and gremlin in the sea anemone Nematostella vectensis: implications for the evolution of axial patterning. , 2006, Developmental biology.

[75]  R. Raff,et al.  Chapter 7. Axis formation and the rapid evolutionary transformation of larval form. , 2009, Current topics in developmental biology.

[76]  Bob Goldstein,et al.  Gastrulation in C. elegans. , 2005, WormBook : the online review of C. elegans biology.

[77]  J. D. Lambert,et al.  Mesoderm in spiralians: the organizer and the 4d cell. , 2008, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[78]  William T. Arthur,et al.  The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology , 1997 .

[79]  Edwin Munro,et al.  Cellular morphogenesis in ascidians: how to shape a simple tadpole. , 2006, Current opinion in genetics & development.

[80]  Grigory Genikhovich,et al.  Early development and axis specification in the sea anemone Nematostella vectensis. , 2007, Developmental biology.

[81]  Thomas C Kaufman,et al.  Short and long germ segmentation: unanswered questions in the evolution of a developmental mode , 2005, Evolution & development.

[82]  J. Henry Conserved mechanism of dorsoventral axis determination in equal-cleaving spiralians. , 2002, Developmental biology.

[83]  Howard C. Blue,et al.  Chapter 7. , 2007 .

[84]  W. Damen,et al.  Evolutionary conservation and divergence of the segmentation process in arthropods , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[85]  M. Leptin,et al.  Gastrulation in Drosophila: the logic and the cellular mechanisms , 1999, The EMBO journal.

[86]  G. Freeman The role of cleavage in the localization of developmental potential in the ctenophore Mnemiopsis leidyi. , 1976, Developmental biology.

[87]  R V Solé,et al.  Phenotypic and dynamical transitions in model genetic networks II. Application to the evolution of segmentation mechanisms , 2001, Evolution & development.

[88]  Isaac Salazar-Ciudad,et al.  Mechanisms of pattern formation in development and evolution , 2003, Development.

[89]  T. Bouwmeester,et al.  The Spemann-Mangold organizer: the control of fate specification and morphogenetic rearrangements during gastrulation in Xenopus. , 2001, The International journal of developmental biology.

[90]  C. H. O'DONOGHUE Traité de zoologie , 1949, Nature.

[91]  Prof. Dr. José A. Campos-Ortega,et al.  The Embryonic Development of Drosophila melanogaster , 1997, Springer Berlin Heidelberg.

[92]  T. Kaufman,et al.  Insect appendages and comparative ontogenetics. , 2005, Developmental biology.

[93]  A. Schier,et al.  A genetic screen for mutations affecting embryogenesis in zebrafish. , 1996, Development.

[94]  E. Davidson,et al.  Origin of Bilaterian Body Plans: Evolution of Developmental Regulatory Mechanisms , 1995, Science.

[95]  Vincent J. Lynch,et al.  Resurrecting the Role of Transcription Factor Change in Developmental Evolution , 2008, Evolution; international journal of organic evolution.

[96]  Isaac Salazar-Ciudad,et al.  A gene network model accounting for development and evolution of mammalian teeth , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[97]  M. Martindale,et al.  Gastrulation in the cnidarian Nematostella vectensis occurs via invagination not ingression. , 2007, Developmental biology.

[98]  G. Forgacs,et al.  Before programs: the physical origination of multicellular forms. , 2006, The International journal of developmental biology.