Arthropod Segmentation: beyond the Drosophila paradigm

Most of our knowledge about the mechanisms of segmentation in arthropods comes from work on Drosophila melanogaster. In recent years it has become clear that this mechanism is far from universal, and different arthropod groups have distinct modes of segmentation that operate through divergent genetic mechanisms. We review recent data from a range of arthropods, identifying which features of the D. melanogaster segmentation cascade are present in the different groups, and discuss the evolutionary implications of their conserved and divergent aspects. A model is emerging, although slowly, for the way that arthropod segmentation mechanisms have evolved.

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

[2]  L. Holland Heads or tails? Amphioxus and the evolution of anterior-posterior patterning in deuterostomes. , 2002, Developmental biology.

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

[4]  R. Sommer,et al.  Segmentation gene expression in the housefly Musca domestica. , 1991, Development.

[5]  R. Lehmann,et al.  Translational regulation of nanos by RNA localization , 1994, Nature.

[6]  Susan J. Brown,et al.  The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[7]  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.

[8]  E C Stephenson,et al.  Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. , 1991, Development.

[9]  M. Schoppmeier,et al.  Expression of Pax group III genes suggests a single‐segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei , 2005, Evolution & development.

[10]  G. Struhl,et al.  A molecular gradient in early Drosophila embryos and its role in specifying the body pattern , 1986, Nature.

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

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

[13]  A. Martinez-Arias,et al.  Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. , 1989, The EMBO journal.

[14]  M. Fujioka,et al.  Analysis of an even-skipped rescue transgene reveals both composite and discrete neuronal and early blastoderm enhancers, and multi-stripe positioning by gap gene repressor gradients. , 1999, Development.

[15]  T. Kaufman,et al.  hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. , 2009, Development.

[16]  C. Nüsslein-Volhard,et al.  A gradient of bicoid protein in Drosophila embryos , 1988, Cell.

[17]  O. Muraoka,et al.  Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. , 2005, Developmental biology.

[18]  R. Lehmann,et al.  A gap gene, hunchback, regulates the spatial expression of Ultrabithorax , 1986, Cell.

[19]  T. Kaufman,et al.  Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica , 2004, Evolution & development.

[20]  M. Kaeberlein,et al.  A genetic screen for zygotic embryonic lethal mutations affecting cuticular morphology in the wasp Nasonia vitripennis. , 2000, Genetics.

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

[22]  R. Denell,et al.  A strategy for mapping bicoid on the phylogenetic tree , 2001, Current Biology.

[23]  Urs Schmidt-Ott,et al.  A single Hox3 gene with composite bicoid and zerknüllt expression characteristics in non-Cyclorrhaphan flies , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

[26]  D. Leaf,et al.  The jewel wasp Nasonia: Querying the genome with haplo‐diploid genetics , 2003, Genesis.

[27]  M. Grbic Polyembryony in parasitic wasps: evolution of a novel mode of development. , 2003, The International journal of developmental biology.

[28]  Bret J. Pearson,et al.  Drosophila Neuroblasts Sequentially Express Transcription Factors which Specify the Temporal Identity of Their Neuronal Progeny , 2001, Cell.

[29]  S. Lall,et al.  Nanos Plays a Conserved Role in Axial Patterning outside of the Diptera , 2003, Current Biology.

[30]  Martin Klingler,et al.  Parental RNAi in Tribolium (Coleoptera) , 2002, Current Biology.

[31]  P. Ingham,et al.  Isolation, structure, and expression of even-skipped: A second pair-rule gene of Drosophila containing a homeo box , 1986, Cell.

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

[33]  S. Omholt,et al.  Specific developmental gene silencing in the honey bee using a homeobox motif , 2002, Insect molecular biology.

[34]  M. Averof,et al.  Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[36]  Gregor Bucher,et al.  Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum , 1998, Development Genes and Evolution.

[37]  S. Roth,et al.  Tribolium embryogenesis: a SEM study of cell shapes and movements from blastoderm to serosal closure , 2000, Development Genes and Evolution.

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

[39]  C. Desplan,et al.  Evolution of Development: Beyond Bicoid , 2003, Current Biology.

[40]  M. Averof,et al.  Ancestral role of caudal genes in axis elongation and segmentation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  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.

[42]  Reinhard Schröder,et al.  The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium , 2003, Nature.

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

[44]  Ralf J. Sommer,et al.  Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera) , 1993, Nature.

[45]  K. Miyawaki,et al.  Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis , 2004, Mechanisms of Development.

[46]  S. Roth,et al.  Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle , 2004, Development Genes and Evolution.

[47]  W. Arthur,et al.  The centipede Strigamia maritima: what it can tell us about the development and evolution of segmentation. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  S. Carroll,et al.  Polyembryonic development: insect pattern formation in a cellularized environment. , 1996, Development.

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

[50]  P. Lawrence,et al.  Parasegments and compartments in the Drosophila embryo , 1985, Nature.

[51]  M. Akam,et al.  Evolution of Ftz protein function in insects , 2001, Current Biology.

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

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

[54]  Yury Goltsev,et al.  Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. , 2004, Developmental biology.

[55]  P. Lawrence Drosophila Unfolded. (Book Reviews: The Making of a Fly. The Genetics of Animal Design.) , 1992 .

[56]  M. Akam,et al.  Cellularization in locust embryos occurs before blastoderm formation. , 1997, Development.

[57]  M. Akam,et al.  Hox genes and the phylogeny of the arthropods , 2001, Current Biology.

[58]  K. Miyawaki,et al.  piggyBac‐mediated somatic transformation of the two‐spotted cricket, Gryllus bimaculatus , 2004, Development, growth & differentiation.

[59]  E. Quéinnec,et al.  hedgehog is a segment polarity gene in a crustacean and a chelicerate , 2004, Development Genes and Evolution.

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

[61]  Gregor Bucher,et al.  Divergent segmentation mechanism in the short germ insect Tribolium revealed by giant expression and function , 2004, Development.

[62]  G. Struhl,et al.  Structure of the Drosophila BicaudalD protein and its role in localizing the posterior determinant nanos , 1989, Cell.

[63]  T. Kaufman,et al.  Krüppel is a gap gene in the intermediate germband insect Oncopeltus fasciatus and is required for development of both blastoderm and germband-derived segments , 2004, Development.

[64]  Susan J. Brown,et al.  Anterior localization of maternal mRNAs in a short germ insect lacking bicoid , 2005, Evolution & development.

[65]  Dierk Niessing,et al.  RNA binding and translational suppression by bicoid , 1996, Nature.

[66]  C. Nüsslein-Volhard,et al.  The origin of pattern and polarity in the Drosophila embryo , 1992, Cell.

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

[68]  H. Jäckle,et al.  The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Gregor Bucher,et al.  Breakdown of abdominal patterning in the Tribolium Krüppel mutant jaws , 2005, Development.

[70]  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.

[71]  H. Taubert,et al.  Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Arthur,et al.  The pattern of variation in centipede segment number as an example of developmental constraint in evolution , 1999, Journal of theoretical biology.

[73]  N. Patel,et al.  Functional conservation of the wingless–engrailed interaction as shown by a widely applicable baculovirus misexpression system , 1999, Current Biology.

[74]  M. Akam,et al.  Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha) , 2004, Evolution & development.

[75]  O. Pourquié The Segmentation Clock: Converting Embryonic Time into Spatial Pattern , 2003, Science.

[76]  J. Shultz,et al.  Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic , 2005, Proceedings of the Royal Society B: Biological Sciences.

[77]  J. Dubnau,et al.  RNA recognition and translational regulation by a homeodomain protein , 1996, Nature.

[78]  R. Janssen,et al.  Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). , 2004, Developmental biology.

[79]  T. Kaufman,et al.  even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect , 2005, Development.

[80]  R. Wharton,et al.  Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in drosophila embryos , 1995, Cell.

[81]  K. Miyawaki,et al.  caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus , 2005, Mechanisms of Development.

[82]  K. Struhl,et al.  The gradient morphogen bicoid is a concentration-dependent transcriptional activator , 1989, Cell.

[83]  G. K. Davis,et al.  Pax3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. , 2005, Developmental biology.

[84]  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.

[85]  H. Okamoto,et al.  Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus , 2005, Development.

[86]  M. Akam,et al.  A Double Segment Periodicity Underlies Segment Generation in Centipede Development , 2004, Current Biology.

[87]  Ruth Lehmann,et al.  The Drosophila posterior-group gene nanos functions by repressing hunchback activity , 1989, Nature.

[88]  G. Odell,et al.  The segment polarity network is a robust developmental module , 2000, Nature.

[89]  Diethard Tautz,et al.  Separable stripe enhancer elements for the pair‐rule gene hairy in the beetle Tribolium , 2004, EMBO reports.

[90]  M. Hülskamp,et al.  Gap genes and gradients – The logic behind the gaps , 1991, BioEssays : news and reviews in molecular, cellular and developmental biology.

[91]  Frietson Galis,et al.  Conservation of the segmented germband stage: robustness or pleiotropy? , 2002, Trends in genetics : TIG.

[92]  Bernhard G Herrmann,et al.  Segmentation in vertebrates: clock and gradient finally joined. , 2004, Genes & development.

[93]  T. Kaufman,et al.  Functional analyses in the milkweed bug Oncopeltus fasciatus (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. , 2005, Developmental biology.

[94]  W. Damen Arthropod Segmentation: Why Centipedes Are Odd , 2004, Current Biology.