Segmentation: mono- or polyphyletic?

Understanding the evolutionary origins of segmented body plans in the metazoa has been a long-standing fascination for scientists. Competing hypotheses explaining the presence of distinct segmented taxa range from the suggestion that all segmentation in the metazoa is homologous to the proposal that segmentation arose independently many times, even within an individual clade or species. A major new source of information regarding the extent of homology vs. homoplasy of segmentation in recent years has been an examination of the extent to which molecular mechanisms underlying the segmentation process are conserved, the rationale being that a shared history will be apparent by the presence of common molecular components of a developmental program that give rise to a segmented body plan. There has been substantial progress recently in understanding the molecular mechanisms underlying the segmentation process in many groups, specifically within the three overtly segmented phyla: Annelida, Arthropoda and Chordata. This review will discuss what we currently know about the segmentation process in each group and how our understanding of the development of segmented structures in distinct taxa have influenced the hypotheses explaining the presence of a segmented body plan in the metazoa.

[1]  F. Falciani,et al.  Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. , 1994, Development.

[2]  R. B. Clark Dynamics in Metazoan Evolution: The Origin of the Coelom and Segments. , 1964 .

[3]  The ancestral cleavage pattern of the clitellates and its phylogenetic deviations , 1999 .

[4]  P. Lawrence The making of a fly , 1992 .

[5]  D. Anderson The Comparative Embryology of the Polychaeta , 1966 .

[6]  O. Pourquié,et al.  Avian hairy Gene Expression Identifies a Molecular Clock Linked to Vertebrate Segmentation and Somitogenesis , 1997, Cell.

[7]  A. Giangrande,et al.  METAMERISM AND LIFE-STYLE WITHIN POLYCHAETES : MORPHO-FUNCTIONAL ASPECTS AND EVOLUTIONARY IMPLICATIONS , 1998 .

[8]  R. Raff,et al.  Evidence for a clade of nematodes, arthropods and other moulting animals , 1997, Nature.

[9]  W. Damen fushi tarazu: A Hox gene changes its role , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[10]  C. Nüsslein-Volhard,et al.  Control of her1 expression during zebrafish somitogenesis by a delta-dependent oscillator and an independent wave-front activity. , 2000, Genes & development.

[11]  Mi Hye Song,et al.  Expression and function of an even-skipped homolog in the leech Helobdella robusta. , 2002, Development.

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

[13]  T. Kaufman,et al.  Exploring the myriapod body plan: expression patterns of the ten Hox genes in a centipede. , 2002, Development.

[14]  Gonzalo Giribet,et al.  Arthropod phylogeny based on eight molecular loci and morphology , 2001, Nature.

[15]  A. Nederbragt,et al.  Expression of Patella vulgata orthologs of engrailed and dpp-BMP2/4 in adjacent domains during molluscan shell development suggests a conserved compartment boundary mechanism. , 2002, Developmental biology.

[16]  C. Kimmel,et al.  Was Urbilateria segmented? , 1996, Trends in genetics : TIG.

[17]  D. Tautz,et al.  Expression patterns of hairy, even-skipped, and runt in the spider Cupiennius salei imply that these genes were segmentation genes in a basal arthropod. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[18]  G. K. Davis,et al.  Short, long, and beyond: molecular and embryological approaches to insect segmentation. , 2002, Annual review of entomology.

[19]  N. Patel The evolution of arthropod segmentation: insights from comparisons of gene expression patterns. , 1994, Development (Cambridge, England). Supplement.

[20]  Mary-Lee Dequéant,et al.  Periodic Notch inhibition by Lunatic Fringe underlies the chick segmentation clock , 2003, Nature.

[21]  I. Ruiz-Trillo,et al.  A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D. McHugh Molecular phylogeny of the Annelida , 2000 .

[23]  M. Akam,et al.  A role for Fringe in segment morphogenesis but not segment formation in the grasshopper, Schistocerca gregaria , 2000, Development Genes and Evolution.

[24]  T. Kaufman,et al.  Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. , 2002, Developmental biology.

[25]  P. Dearden,et al.  Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae , 2002, Development.

[26]  N. Patel,et al.  Serially homologous engrailed stripes are generated via different cell lineages in the germ band of amphipod crustaceans (Malacostraca, Peracarida). , 1994, The International journal of developmental biology.

[27]  W. Damen Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. , 2002, Development.

[28]  K. Peterson,et al.  Animal phylogeny and the ancestry of bilaterians: inferences from morphology and 18S rDNA gene sequences , 2001, Evolution & development.

[29]  G. K. Davis,et al.  Playing by pair-rules? , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[30]  L. Holland,et al.  Developmental expression of AmphiWnt1, an amphioxus gene in the Wnt1/wingless subfamily , 2000, Development Genes and Evolution.

[31]  R. Sommer,et al.  Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. , 1995, Development.

[32]  Yoshiaki Suzuki,et al.  Double‐segment defining role of even‐skipped homologs along the evolution of insect pattern formation , 1997, Development, growth & differentiation.

[33]  M. Capecchi,et al.  Hoxc13 mutant mice lack external hair. , 1998, Genes & development.

[34]  E. Robertis,et al.  The ancestry of segmentation , 1997, Nature.

[35]  Nipam H. Patel,et al.  Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles , 1994, Nature.

[36]  M. Jackson,et al.  Origin of the Metazoa , 1979, Nature.

[37]  S. Morris,et al.  Middle Cambrian Polychaetes from the Burgess Shale of British Columbia , 1979 .

[38]  J. Iwasa,et al.  The leech hunchback protein is expressed in the epithelium and CNS but not in the segmental precursor lineages , 2000, Development Genes and Evolution.

[39]  N. Patel,et al.  Expression of engrailed during segmentation in grasshopper and crayfish. , 1989, Development.

[40]  K. G. Coleman,et al.  Expression of engrailed proteins in arthropods, annelids, and chordates. , 1989, Cell.

[41]  D. Weisblat,et al.  Gangliogenesis in leech: morphogenetic processes leading to segmentation in the central nervous system , 1998, Development Genes and Evolution.

[42]  J. Campos-Ortega,et al.  Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites. , 1996, Development.

[43]  E. Herniou,et al.  Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. , 1999, Science.

[44]  G. Budd Why are arthropods segmented? , 2001, Evolution & development.

[45]  K. Sander Specification of the Basic Body Pattern in Insect Embryogenesis1 , 1976 .

[46]  H. Jäckle,et al.  Drosophila mode of metamerization in the embryogenesis of the lepidopteran insect Manduca sexta. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[47]  M. Shankland,et al.  Leech segmental repeats develop normally in the absence of signals from either anterior or posterior segments. , 2000, Developmental biology.

[48]  C. Simon,et al.  Polychaetes , 2002 .

[49]  Y. Sasai,et al.  A common plan for dorsoventral patterning in Bilateria , 1996, Nature.

[50]  N. Patel,et al.  Analysis of the expression pattern of Mysidium columbiae wingless provides evidence for conserved mesodermal and retinal patterning processes among insects and crustaceans , 2002, Development Genes and Evolution.

[51]  Takashi Shimizu,et al.  Expression of hunchback protein in a subset of ectodermal teloblasts of the oligochaete annelid Tubifex , 2002, Development Genes and Evolution.

[52]  William C. Smith,et al.  An ascidian engrailed gene , 2002, Development Genes and Evolution.

[53]  N. Williams,et al.  Sequence and embryonic expression of the amphioxus engrailed gene (AmphiEn): the metameric pattern of transcription resembles that of its segment-polarity homolog in Drosophila. , 1997, Development.

[54]  Nipam H. Patel,et al.  Changing role of even-skipped during the evolution of insect pattern formation , 1992, Nature.

[55]  L. Nagy,et al.  The role of wingless in the development of multibranched crustacean limbs , 1999, Development Genes and Evolution.

[56]  M. Shankland,et al.  Identification and characterization of a hunchback orthologue, Lzf2, and its expression during leech embryogenesis. , 1996, Developmental biology.

[57]  Evolutionary biology: Hedgehog crosses the snail's midline , 2002, Nature.

[58]  E. D. De Robertis Evolutionary biology. The ancestry of segmentation. , 1997, Nature.

[59]  W. F. Gutmann Relationships Between Invertebrate Phyla Based on Functional-Mechanical Analysis of the Hydrostatic Skeleton , 1981 .

[60]  G. Wray,et al.  Evolution of regeneration and fission in annelids: insights from engrailed- and orthodenticle-class gene expression. , 2001, Development.

[61]  Y. Saga,et al.  The making of the somite: molecular events in vertebrate segmentation , 2001, Nature Reviews Genetics.

[62]  Çîîëîãèÿ áåñïîçâîíî÷íûõ,et al.  Invertebrate Zoology , 1927, Nature.

[63]  D. Arendt,et al.  Arthropod-like Expression Patterns of engrailed and wingless in the Annelid Platynereis dumerilii Suggest a Role in Segment Formation , 2003, Current Biology.

[64]  M. Shankland,et al.  Establishment of segment polarity in the ectoderm of the leech Helobdella. , 2001, Development.

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

[66]  Helen Arthur,et al.  The pattern of segment formation, as revealed by engrailed expression, in a centipede with a variable number of segments , 2003, Evolution & development.

[67]  M. Telford,et al.  Evidence for the derivation of the Drosophila fushi tarazu gene from a Hox gene orthologous to lophotrochozoan Lox5 , 2000, Current Biology.

[68]  D. Weisblat,et al.  Segmental expression of an engrailed-class gene during early development and neurogenesis in an annelid. , 1991, Development.

[69]  S. Boissinot,et al.  Evolutionary Biology , 2000, Evolutionary Biology.

[70]  Sean B. Carroll,et al.  Hox genes in brachiopods and priapulids and protostome evolution , 1999, Nature.

[71]  A. Mccarthy Development , 1996, Current Opinion in Neurobiology.

[72]  Arthropod Relationships , 1998, The Systematics Association Special Volume Series.

[73]  D. Eernisse,et al.  Annelida and Arthropoda are Not Sister Taxa: A Phylogenetic Analysis of Spiralian Metazoan Morphology , 1992 .

[74]  D. Weisblat,et al.  A hedgehog homolog regulates gut formation in leech (Helobdella) , 2003, Development.

[75]  R. Sandeman,et al.  Expression of engrailed can be lost and regained in cells of one clone in crustacean embryos. , 1993, The International journal of developmental biology.

[76]  M. Akam,et al.  Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, decapentaplegic and caudal expression. , 2001, Development.

[77]  R. Marco,et al.  Genomic organization and developmental pattern of expression of the engrailed gene from the brine shrimp Artemia. , 1993, Development.

[78]  D. Weisblat,et al.  Cell lineage analysis of the expression of an engrailed homolog in leech embryos. , 1993, Development.

[79]  Michael Schoppmeier,et al.  Involvement of Notch and Delta genes in spider segmentation , 2003, Nature.

[80]  J. Lake,et al.  Evidence from 18S ribosomal DNA that the lophophorates are protostome animals , 1995, Science.

[81]  M. Martindale,et al.  The spatial and temporal expression of Ch-en, the engrailed gene in the polychaete Chaetopterus, does not support a role in body axis segmentation. , 2001, Developmental biology.

[82]  D. Tautz,et al.  Mitochondrial protein phylogeny joins myriapods with chelicerates , 2001, Nature.

[83]  Takashi Shimizu,et al.  Segmentation in Annelids: Cellular and Molecular Basis for Metameric Body Plan , 2001 .

[84]  P. Whitington,et al.  Segmentally iterated expression of an engrailed-class gene in the embryo of an australian onychophoran , 1997, Development Genes and Evolution.

[85]  A. H. Werbrock,et al.  A polychaete hunchback ortholog. , 2001, Developmental biology.

[86]  D. Weisblat,et al.  Cell lineage and segmentation in the leech. , 1985, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[87]  S. Carroll,et al.  Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum , 1994, Nature.

[88]  S. Lall,et al.  Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. , 2001, Development.

[89]  M. Martindale,et al.  Origin of segmental identity in the development of the leech nervous system. , 1991, Development (Cambridge, England). Supplement.

[90]  G. Scholtz The Articulata hypothesis – or what is a segment? , 2002 .

[91]  R. Raff Understanding Evolution: The Next Step. (Book Reviews: The Shape of Life. Genes, Development, and the Evolution of Animal Form.) , 1996 .

[92]  W. Dohle,et al.  The cleavage pattern in the leech Theromyzon tessulatum (Hirudinea, Glossiphoniidae) , 1988, Journal of morphology.

[93]  Diethard Tautz,et al.  Regulation of the Drosophila segmentation gene hunchback by two maternal morphogenetic centres , 1988, Nature.

[94]  Susan J. Brown,et al.  Molecular characterization and embryonic expression of the even-skipped ortholog of Tribolium castaneum , 1997, Mechanisms of Development.

[95]  J. Boore,et al.  The mitochondrial genome of the Sipunculid Phascolopsis gouldii supports its association with Annelida rather than Mollusca. , 2002, Molecular biology and evolution.

[96]  G. Balavoine,et al.  One or Three Cambrian Radiations? , 1998, Science.

[97]  M. Telford,et al.  Combined large and small subunit ribosomal RNA phylogenies support a basal position of the acoelomorph flatworms , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[98]  Christian Wehrle,et al.  Wnt3a plays a major role in the segmentation clock controlling somitogenesis. , 2003, Developmental cell.

[99]  G. K. Davis,et al.  Pax group III genes and the evolution of insect pair-rule patterning. , 2001, Development.

[100]  D. Weisblat,et al.  Segmentation in leech development. , 1988, Development.

[101]  Y. Misumi,et al.  Correlation of diversity of leg morphology in Gryllus bimaculatus (cricket) with divergence in dpp expression pattern during leg development. , 2000, Development.

[102]  G. D,et al.  American Naturalist , 1867, Nature.

[103]  Prof. P. P. Iwanoff Die entwicklung der larvalsegmente bei den anneliden , 1928, Zeitschrift für Morphologie und Ökologie der Tiere.

[104]  D. Weisblat,et al.  An overview of glossiphoniid leech development , 2001 .