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  • Review Article
  • Published:

Arthropod Segmentation: beyond the Drosophila paradigm

Nature Reviews Genetics volume 6, pages 905–916 (2005)Cite this article

Key Points

  • The segmentation cascade of Drosophila melanogaster is not typical of arthropod segmentation in general, although many of its features are present in other arthropod groups to some extent.

  • The earliest stage of the cascade — the maternal-effect genes — has diverged significantly; for example, bicoid function is specific to higher Diptera.

  • In insects other than D. melanogaster gap-gene homologues function in determining segmental identity, but the details and specific roles of each gene have diverged. It is possible that the ancestral role of gap genes was to regulate Hox genes, and that these genes were later recruited to regulate segmentation genes.

  • At least one pair-rule gene homologue is expressed in a pattern that is consistent with its involvement in segmentation in every arthropod species that has been studied. However, pair-rule periodicity has only been found in a few cases, and could have evolved independently in different lineages.

  • The segment polarity gene network is the most conserved aspect of the segmentation cascade. engrailed is involved in defining segmental boundaries in every arthropod species that has been studied.

  • There is evidence that the Notch signalling pathway is involved in arthropod segmentation, through a segmentation oscillator that bears many similarities to the vertebrate somitogenesis clock. The oscillator could be an ancestral feature that has been lost in the lineage leading to higher insects.

  • The advent of RNAi and transgenesis in non-model arthropods provides the opportunity for functional studies that could extend the understanding of arthropod segmentation beyond the D. melanogaster model.

  • Although a model is emerging for how arthropod segmentation evolved, many unanswered questions remain; more data on a wider range of arthropods is needed before the model will be complete.

Abstract

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.

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Figure 1: Conservation of the segmentation cascade in arthropods.
Figure 2: Phylogenetic relationships between the arthropod species discussed in this article.
Figure 3: A comparison of hunchback expression and function in two sequentially segmenting insects.

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References

  1. Aguinaldo, A. M. et al. Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489–493 (1997).

    Article  CAS  PubMed  Google Scholar 

  2. Stollewerk, A., Schoppmeier, M. & Damen, W. G. M. Involvement of Notch and Delta genes in spider segmentation. Nature 423, 863–865 (2003). The first report of the involvement of the Notch signalling pathway in segmentation in any arthropod species.

    Article  CAS  PubMed  Google Scholar 

  3. Schoppmeier, M. & Damen, W. G. M. Suppressor of Hairless and Presenilin phenotypes imply involvement of canonical Notch-signalling in segmentation of the spider Cupiennius salei. Dev. Biol. 280, 211–224 (2005).

    Article  CAS  PubMed  Google Scholar 

  4. Lawrence, P. A. The Making of a Fly: the Genetics of Animal Design (Blackwell Scientific, Oxford, UK, 1992).

    Google Scholar 

  5. Maderspacher, F., Bucher, G. & Klingler, M. Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum. Dev. Genes Evol. 208, 558–568 (1998).

    Article  CAS  PubMed  Google Scholar 

  6. Pultz et al. A genetic screen for zygotic embryonic lethal mutations affecting cuticular morphology in the wasp Nasonia vitripennis. Genetics 154, 1213–1229 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Pultz, M. A. & Leaf, D. S. The jewel wasp Nasonia: querying the genome with haplo-diploid genetics. Genesis 35, 185–191 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Bucher, G., Scholten, J. & Klingler, M. Parental RNAi in Tribolium (Coleoptera). Curr. Biol. 12, R85–R86 (2002). A report on the application of parental RNAi in a non-model arthropod species. This technique has since been used successfully in several other species.

    Article  CAS  PubMed  Google Scholar 

  9. Eckert, C., Aranda, M., Wolff, C. & Tautz, D. Separable stripe enhancer elements for the pair-rule gene hairy in the beetle Tribolium. EMBO Rep. 5, 638–642 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Pavlopoulos, A. & Averof, M. Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. Proc. Natl Acad. Sci. USA 102, 7888–7893 (2005). This article reports the first example of genetic transformation in the crustacean Parhyale hawaiiensis . This is one of very few species, and the only non-insect arthropod, for which this technique has been developed.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Shinmyo, Y. et al. piggyBac-mediated somatic transformation of the two-spotted cricket, Gryllus bimaculatus. Dev. Growth Differ. 46, 343–349 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. Raff, R. A. The Shape of Life: Genes, Development, and the Evolution of Animal Form (Univ. Chicago Press, Chicago, 1996).

    Book  Google Scholar 

  13. Martinez-Arias, A. & Lawrence, P. A. Parasegments and compartments in the Drosophila embryo. Nature 313, 639–642 (1985).

    Article  CAS  PubMed  Google Scholar 

  14. Damen, W. G. Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129, 1239–1250 (2002).

    CAS  PubMed  Google Scholar 

  15. von Dassow, G., Meir, E., Munro, E. M. & Odell, G. M. The segment polarity network is a robust developmental module. Nature 406, 188–192 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Simonnet, F., Deutsch, J. & Queinnec, E. hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev. Genes Evol. 214, 537–545 (2004).

    Article  CAS  PubMed  Google Scholar 

  17. Hughes, C. L. & Kaufman, T. C. Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev. Biol. 247, 47–61 (2002).

    Article  CAS  PubMed  Google Scholar 

  18. Nagy, L. M. & Carroll, S. Conservation of wingless patterning functions in the short-germ embryos of Tribolium castaneum. Nature 367, 460–463 (1994).

    Article  CAS  PubMed  Google Scholar 

  19. Dearden, P. K. & Akam, M. Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, decapentaplegic and caudal expression. Development 128, 3435–3444 (2001).

    CAS  PubMed  Google Scholar 

  20. Janssen, R., Prpic, N.-M. & Damen, W. G. M. Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev. Biol. 268, 89–104 (2004).

    Article  CAS  PubMed  Google Scholar 

  21. Galis, F., van Dooren, T. J. & Metz, J. A. Conservation of the segmented germband stage: robustness or pleiotropy? Trends Genet. 18, 504–509 (2002).

    Article  CAS  PubMed  Google Scholar 

  22. Oppenheimer, D. I., MacNicol, A. M. & Patel, N. H. Functional conservation of the wingless–engrailed interaction as shown by a widely applicable baculovirus misexpression system. Curr. Biol. 9, 1288–1296 (1999).

    Article  CAS  PubMed  Google Scholar 

  23. Beye, M., Hartel, S., Hagen, A., Hasselmann, M. & Omholt, S. W. Specific developmental gene silencing in the honey bee using a homeobox motif. Insect Mol. Biol. 11, 527–532 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. Davis, G. K. & Patel, N. H. Short, long, and beyond: molecular and embryological approaches to insect segmentation. Ann. Rev. Entomol. 47, 669–699 (2002).

    Article  CAS  Google Scholar 

  25. Bucher, G. & Klingler, M. Divergent segmentation mechanism in the short germ insect Tribolium revealed by giant expression and function. Development 131, 1729–1740 (2004).

    Article  CAS  PubMed  Google Scholar 

  26. Schröder, R. The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422, 621–625 (2003). A functional analysis of the gap gene hunchback in the beetle T. castaneum . This analysis can be compared to that of the milkweed bug in reference 32.

    Article  CAS  PubMed  Google Scholar 

  27. Grbic, M. Polyembryony in parasitic wasps: evolution of a novel mode of development. Int. J. Dev. Biol. 47, 633–642 (2003).

    PubMed  Google Scholar 

  28. Shinmyo, Y. et al. caudal is required for gnathal and thoracic patterning and for posterior elongation in the intermediate-germband cricket Gryllus bimaculatus. Mech. Dev. 122, 231–239 (2005).

    Article  CAS  PubMed  Google Scholar 

  29. Miyawaki, K. et al. Involvement of Wingless/Armadillo signaling in the posterior sequential segmentation in the cricket, Gryllus bimaculatus (Orthoptera), as revealed by RNAi analysis. Mech. Dev. 121, 119–130 (2004).

    Article  CAS  PubMed  Google Scholar 

  30. Mito, T. et al. Non-canonical functions of hunchback in segment patterning of the intermediate germ cricket Gryllus bimaculatus. Development 132, 2069–2079 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. Liu, P. Z. & Kaufman, T. C. even-skipped is not a pair-rule gene but has segmental and gap-like functions in Oncopeltus fasciatus, an intermediate germband insect. Development 132, 2081–2092 (2005).

    Article  CAS  PubMed  Google Scholar 

  32. Liu, P. Z. & Kaufman, T. C. hunchback is required for suppression of abdominal identity, and for proper germband growth and segmentation in the intermediate germband insect Oncopeltus fasciatus. Development 131, 1515–1527 (2004). A functional analysis of the gap gene hunchback in the milkweed bug O. fasciatus . This analysis can be compared to that of the beetle T. castaneum in reference 26.

    Article  CAS  PubMed  Google Scholar 

  33. Liu, P. Z. & Kaufman, T. C. Krüppel is a gap gene in the intermediate germband insect Oncopeltus fasciatus and is required for development of both blastoderm and germband-derived segments. Development 131, 4567–4579 (2004). A functional analysis of the gap gene Krüppel in O. fasciatus.

    Article  CAS  PubMed  Google Scholar 

  34. Angelini, D. R. & Kaufman, T. C. Functional analyses in the milkweed bug Oncopeltus fasciatus (Hemiptera) support a role for Wnt signaling in body segmentation but not appendage development. Dev. Biol. 283, 409–423 (2005).

    Article  CAS  PubMed  Google Scholar 

  35. Copf, T., Schroder, R. & Averof, M. Ancestral role of caudal genes in axis elongation and segmentation. Proc. Natl Acad. Sci. USA 101, 17711–17715 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Regier, J. C., Shultz, J. W. & Kambic, R. E. Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proc. Biol. Sci. 272, 395–401 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Cook, C. E., Smith, M. L., Telford, M. J., Bastianello, A. & Akam, M. Hox genes and the phylogeny of the arthropods. Curr. Biol. 11, 759–763 (2001).

    Article  CAS  PubMed  Google Scholar 

  38. Schoppmeier, M. & Damen, W. G. M. Expression of Pax group III genes suggests a single-segmental periodicity for opisthosomal segment patterning in the spider Cupiennius salei. Evol. Dev. 7, 160–169 (2005). This study shows that the Pax group III genes — one member of which is a pair-rule gene in D. melanogaster — are expressed with a single-segment periodicity in a chelicerate.

    Article  CAS  PubMed  Google Scholar 

  39. Damen, W. G., Weller, M. & Tautz, D. Expression patterns of hairy, even-skipped, and runt in the spider Cupiennius salei imply that these genes were segmentation genes in a basal arthropod. Proc. Natl Acad. Sci. USA 97, 4515–4519 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Dearden, P. K., Donly, C. & Grbic, M. Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129, 5461–5472 (2002). The authors show that at least one homologue of a D. melanogaster pair-rule gene is expressed with a double-segment periodicity in the prosoma of a chelicerate.

    Article  CAS  PubMed  Google Scholar 

  41. Chipman, A. D., Arthur, W. & Akam, M. Early development and segment formation in the centipede Strigamia maritima (Geophilomorpha). Evol. Dev. 6, 78–89 (2004).

    Article  PubMed  Google Scholar 

  42. Chipman, A. D., Arthur, W. & Akam, M. A double segment periodicity underlies segment generation in centipede development. Curr. Biol. 14, 1250–1255 (2004). The authors show that caudal and an odd-skipped -related gene are expressed with a double-segment periodicity, and suggest an involvement of the Notch signalling pathway in centipede segmentation.

    Article  CAS  PubMed  Google Scholar 

  43. Driever, W. & Nusslein-Volhard, C. A gradient of bicoid protein in Drosophila embryos. Cell 54, 83–93 (1988).

    Article  CAS  PubMed  Google Scholar 

  44. Struhl, G., Struhl, K. & Macdonald, P. M. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell 57, 1259–1273 (1989).

    Article  CAS  PubMed  Google Scholar 

  45. Wharton, R. P. & Struhl, G. Structure of the Drosophila BicaudalD protein and its role in localizing the the posterior determinant nanos. Cell 59, 881–892 (1989).

    Article  CAS  PubMed  Google Scholar 

  46. Pokrywka, N. J. & Stephenson, E. C. Microtubules mediate the localization of bicoid RNA during Drosophila oogenesis. Development 113, 55–66 (1991).

    CAS  PubMed  Google Scholar 

  47. Irish, V., Lehmann, R. & Akam, M. The Drosophila posterior-group gene nanos functions by repressing hunchback activity. Nature 338, 646–648 (1989).

    Article  CAS  PubMed  Google Scholar 

  48. Murata, Y. & Wharton, R. P. Binding of pumilio to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80, 747–756 (1995).

    Article  CAS  PubMed  Google Scholar 

  49. Gavis, E. R. & Lehmann, R. Translational regulation of nanos by RNA localization. Nature 369, 315–318 (1994).

    Article  CAS  PubMed  Google Scholar 

  50. St Johnston, D. & Nusslein-Volhard, C. The origin of pattern and polarity in the Drosophila embryo. Cell 68, 201–219 (1992).

    Article  CAS  PubMed  Google Scholar 

  51. Sommer, R. & Tautz, D. Segmentation gene expression in the housefly Musca domestica. Development 113, 419–430 (1991).

    CAS  PubMed  Google Scholar 

  52. Stauber, M., Taubert, H. & Schmidt-Ott, U. Function of bicoid and hunchback homologs in the basal cyclorrhaphan fly Megaselia (Phoridae). Proc. Natl Acad. Sci. USA 97, 10844–10849 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Stauber, M., Prell, A. & Schmidt-Ott, U. A single Hox3 gene with composite bicoid and zerknullt expression characteristics in non-Cyclorrhaphan flies. Proc. Natl Acad. Sci. USA 99, 274–279 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Stauber, M., Jackle, H. & Schmidt-Ott, U. The anterior determinant bicoid of Drosophila is a derived Hox class 3 gene. Proc. Natl Acad. Sci. USA 96, 3786–3789 (1999). The first report that bicoid is a derived Hox gene, and that it might be specific to Diptera.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Brown, S. et al. A strategy for mapping bicoid on the phylogenetic tree. Curr. Biol. 11, R43–R44 (2001).

    Article  CAS  PubMed  Google Scholar 

  56. Lynch, J. & Desplan, C. Evolution of development: beyond bicoid. Curr. Biol. 13, R557–R559 (2003).

    Article  CAS  PubMed  Google Scholar 

  57. Handel, K., Grunfelder, C. G., Roth, S. & Sander, K. Tribolium embryogenesis: a SEM study of cell shapes and movements from blastoderm to serosal closure. Dev. Genes Evol. 210, 167–179 (2000).

    Article  CAS  PubMed  Google Scholar 

  58. Handel, K., Basal, A., Fan, X. & Roth, S. Tribolium castaneum twist: gastrulation and mesoderm formation in a short-germ beetle. Dev. Genes Evol. 215, 13–31 (2005). This paper describes the origin and behaviour of mesodermal cells during development in the flour beetle. More data of this kind are needed.

    Article  PubMed  Google Scholar 

  59. Wolff, C., Sommer, R., Schroder, R., Glaser, G. & Tautz, D. Conserved and divergent expression aspects of the Drosophila segmentation gene hunchback in the short germ band embryo of the flour beetle Tribolium. Development 121, 4227–4236 (1995).

    CAS  PubMed  Google Scholar 

  60. Bucher, G., Farzana, L., Brown, S. J. & Klingler, M. Anterior localization of maternal mRNAs in a short germ insect lacking bicoid. Evol. Dev. 7, 142–149 (2005).

    Article  CAS  PubMed  Google Scholar 

  61. Ho, K., Dunin-Borkowski, O. M. & Akam, M. Cellularization in locust embryos occurs before blastoderm formation. Development 124, 2761–2768 (1997).

    CAS  PubMed  Google Scholar 

  62. Lall, S., Ludwig, M. Z. & Patel, N. H. Nanos plays a conserved role in axial patterning outside of the diptera. Curr. Biol. 13, 224–229 (2003).

    Article  CAS  PubMed  Google Scholar 

  63. Sander, K. Specification of the basic body pattern in insect embryogenesis. Adv. Insect Physiol. 12, 125–238 (1976).

    Article  Google Scholar 

  64. Dubnau, J. & Struhl, G. RNA recognition and translational regulation by a homeodomain protein. Nature 379, 694–699 (1996).

    Article  CAS  PubMed  Google Scholar 

  65. Rivera-Pomar, R., Niessing, D., Schmidt-Ott, U., Gehring, W. J. & Jackle, H. RNA binding and translational suppression by bicoid. Nature 379, 746–749 (1996).

    Article  CAS  PubMed  Google Scholar 

  66. Macdonald, P. M. & Struhl, G. A molecular gradient in early Drosophila embryos and its role in specifying the body pattern. Nature 324, 537–545 (1986).

    Article  CAS  PubMed  Google Scholar 

  67. Hulskamp, M. & Tautz, D. Gap genes and gradients — the logic behind the gaps. Bioessays 13, 261–268 (1991).

    Article  CAS  PubMed  Google Scholar 

  68. Fujioka, M., Emi-Sarker, Y., Yusibova, G. L., Goto, T. & Jaynes, J. B. 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. Development 126, 2527–2538 (1999).

    CAS  PubMed  Google Scholar 

  69. Irish, V. F., Martinez-Arias, A. & Akam, M. Spatial regulation of the Antennapedia and Ultrabithorax homeotic genes during Drosophila early development. EMBO J. 8, 1527–1537 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. White, R. A. & Lehmann, R. A gap gene, hunchback, regulates the spatial expression of Ultrabithorax. Cell 47, 311–321 (1986).

    Article  CAS  PubMed  Google Scholar 

  71. Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511–521 (2001).

    Article  CAS  PubMed  Google Scholar 

  72. Goltsev, Y., Hsiong, W., Lanzaro, G. & Levine, M. Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev. Biol. 275, 435–446 (2004). The authors show that homologous posterior pair-rule stripes of expression are probably regulated by a different spatial combination of gap-gene repressors in Anopheles gambiae , when compared with Drosophila melanogaster.

    Article  CAS  PubMed  Google Scholar 

  73. Patel, N. H. et al. Grasshopper hunchback expression reveals conserved and novel aspects of axis formation and segmentation. Development 128, 3459–3472 (2001).

    CAS  PubMed  Google Scholar 

  74. Davis, G. K., D'alessio, J. A. & Patel, N. H. Pax3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. Dev. Biol. 285, 169–184 (2005). A description of the Pax3/7 family of pair-rule gene homologues in various arthropod classes, with a discussion of their ancestral function.

    Article  CAS  PubMed  Google Scholar 

  75. Davis, G. K., Jaramillo, C. A. & Patel, N. H. Pax group III genes and the evolution of insect pair-rule patterning. Development 128, 3445–3458 (2001).

    CAS  PubMed  Google Scholar 

  76. Grbic, M., Nagy, L. M., Carroll, S. B. & Strand, M. Polyembryonic development: insect pattern formation in a cellularized environment. Development 122, 795–804 (1996).

    CAS  PubMed  Google Scholar 

  77. Patel, N. H., Ball, E. E. & Goodman, C. S. Changing role of even-skipped during the evolution of insect pattern formation. Nature 357, 339–342 (1992).

    Article  CAS  PubMed  Google Scholar 

  78. Patel, N. H., Condron, B. G. & Zinn, K. Pair-rule expression patterns of even-skipped are found in both short- and long-germ beetles. Nature 367, 429–434 (1994).

    Article  CAS  PubMed  Google Scholar 

  79. Sommer, R. J. & Tautz, D. Involvement of an orthologue of the Drosophila pair-rule gene hairy in segment formation of the short germ-band embryo of Tribolium (Coleoptera). Nature 361, 448–450 (1993).

    Article  CAS  PubMed  Google Scholar 

  80. Macdonald, P. M., Ingham, P. & Struhl, G. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell 47, 721–734 (1986).

    Article  CAS  PubMed  Google Scholar 

  81. Schröder, R., Jay, D. G. & Tautz, D. Elimination of EVE protein by CALI in the short germ band insect Tribolium suggests a conserved pair-rule function for even skipped. Mech. Dev. 80, 191–195 (1999).

    Article  PubMed  Google Scholar 

  82. Dawes, R., Dawson, I., Falciani, F., Tear, G. & Akam, M. Dax, a locust Hox gene related to fushi-tarazu but showing no pair-rule expression. Development 120, 1561–1572 (1994).

    CAS  PubMed  Google Scholar 

  83. Hughes, C. L., Liu, P. Z. & Kaufman, T. C. Expression patterns of the rogue Hox genes Hox3/zen and fushi tarazu in the apterygote insect Thermobia domestica. Evol. Dev. 6, 393–401 (2004).

    Article  CAS  PubMed  Google Scholar 

  84. Alonso, C. R., Maxton-Kuechenmeister, J. & Akam, M. Evolution of Ftz protein function in insects. Curr. Biol. 11, 1473–1478 (2001).

    Article  CAS  PubMed  Google Scholar 

  85. Brown, S. J., Hilgenfeld, R. B. & Denell, R. E. The beetle Tribolium castaneum has a fushi tarazu homolog expressed in stripes during segmentation. Proc. Natl Acad. Sci. USA 91, 12922–12926 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Arthur, W. & Chipman, A. D. The centipede Strigamia maritima: what it can tell us about the development and evolution of segmentation. Bioessays 27, 653–660 (2005).

    Article  PubMed  Google Scholar 

  87. Damen, W. G. Arthropod segmentation: why centipedes are odd. Curr. Biol. 14, R557–R559 (2004).

    Article  CAS  PubMed  Google Scholar 

  88. Arthur, W. & Farrow, M. The pattern of variation in centipede segment number as an example of developmental constraint in evolution. J. Theor. Biol. 200, 183–191 (1999).

    Article  CAS  PubMed  Google Scholar 

  89. Tautz, D. Segmentation. Dev. Cell 7, 301–312 (2004).

    Article  CAS  PubMed  Google Scholar 

  90. Aulehla, A. & Herrmann, B. G. Segmentation in vertebrates: clock and gradient finally joined. Genes Dev. 18, 2060–2067 (2004).

    Article  CAS  PubMed  Google Scholar 

  91. Aulehla, A. et al. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev. Cell 4, 395–406 (2003).

    Article  CAS  PubMed  Google Scholar 

  92. Shimizu, T., Bae, Y. K., Muraoka, O. & Hibi, M. Interaction of Wnt and caudal-related genes in zebrafish posterior body formation. Dev. Biol. 279, 125–141 (2005).

    Article  CAS  PubMed  Google Scholar 

  93. Holland, L. Z. Heads or tails? Amphioxus and the evolution of anterior–posterior patterning in deuterostomes. Dev. Biol. 241, 209–228 (2002).

    Article  CAS  PubMed  Google Scholar 

  94. Pourquie, O. The segmentation clock: converting embryonic time into spatial pattern. Science 328–330 (2003).

  95. Cerny, A., Bucher, G., Schroder, R. & Klingler, M. Breakdown of abdominal patterning in the Tribolium Krüppel mutant jaws. Development (in the press).

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Authors and Affiliations

  1. Department of Zoology, University Museum of Zoology, Downing Street, Cambridge, CB2 3EJ, UK

    Andrew D. Peel, Ariel D. Chipman & Michael Akam

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  1. Andrew D. Peel
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  2. Ariel D. Chipman
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  3. Michael Akam
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Correspondence to Michael Akam.

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DATABASES

Entrez Gene

bcd

CAD

en

eve

ftz

gt

h

hh

kni

Kr

nos

prd

run

tll

wg

zen

Glossary

MACROEVOLUTION

Evolutionary processes that lead to significant morphological change. This usually refers to processes that occur above the species level.

LIFE HISTORY

The sum of the morphological stages and the ecological environments that an organism goes through during its life.

BILATERIANS

Members of the animal kingdom that have bilateral symmetry — the property of having two similar sides, with definite upper and lower surfaces, and anterior and posterior ends.

DEUTEROSTOMES

One of the three main branches of the bilaterian animals. The deuterostomes include chordates, hemichordates and echinoderms.

LOPHOTROCHOZOANS

One of the three main branches of the bilaterian animals. Lophotrochozoans include annelids, molluscs, flatworms and several other smaller phyla.

ECDYSOZOANS

One of the three main branches of the bilaterian animals. Ecdysozoans are characterized by an unciliated integument, and grow by ecdysis, or moulting. They include nematodes, arthropods and many other smaller phyla.

SOMITOGENESIS

The process of progressive formation, during embryogenesis, of metameric mesodermal units (somites) that represent the precursor structures of dermis, skeletal muscles and the axial skeleton.

BLASTODERM

The layer of cells that completely surrounds an internal mass of yolk in an arthropod embryo.

FOLLICLE CELLS

The somatic cells in Drosophila melanogaster that surround the oocyte; they provide patterning signals to the oocyte and secrete the egg-shell.

DERIVED

Having undergone significant evolutionary change relative to the ancestral state.

GERM BAND

In an arthropod embryo, this is the differentiated portion, which has a distinct anterior–posterior axis, and is where the segmentation process takes place.

SEGMENT POLARITY GENES

A group of genes that define different parts of each segmental repeat. When segment polarity genes are mutated the normal number of segments is formed, but these show internal pattern replication and polarity reversals.

PARASEGMENT

The initial segmental unit that is formed during the segmentation process. The final segment boundaries lie in the middle of the parasegments.

HOLOMETABOLOUS

Insects for which the life cycle includes distinct larvae, pupae and (usually) winged adults.

SYNCYTIUM

A population of nuclei that are not separated by cell membranes. It is typical of the developing blastoderm in Drosophila melanogaster.

SHORT GERM

A mode of insect development in which anterior segments are patterned in the blastoderm, with posterior segments forming sequentially from a cellularized growth zone after gastrulation.

HEMIMETABOLOUS

Insects for which the life cycle includes several larval stages, ending in a sexually mature, winged adult, without going through a pupal stage.

MALACOSTRACANS

A subclass of crustaceans that includes shrimps, lobsters and sandhoppers.

AMPHIPODS

An order of malacostracan crustaceans that includes beachhoppers.

PRE-GNATHAL SEGMENTS

The gnathal segments comprise the mandibular, maxillary and labial head segments of insects. The pre-gnathal segments lie anterior to these segments. The number of pre-gnathal segments has been debated, but probably includes at least three: the ocular, antennal and intercalary segments.

BLASTODISC

An undifferentiated single-cell layer in an arthropod embryo that ultimately gives rise to all embryonic structures.

HOX GENES

A family of homeodomain transcription factors that are conserved across bilaterian animals; they are expressed in sequence along the A–P axis and are involved in conferring axial identity.

PROSOMA

The anterior part of the body in chelicerates, including the head, the mouthparts and the walking legs.

OPISTHOSOMA

The posterior part of the body in chelicerates. It does not include any walking legs.

GEOPHILOMORPHS

A group of centipedes, normally soil dwelling, that are characterized by a long, thin body made up of many segments (27–191).

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Peel, A., Chipman, A. & Akam, M. Arthropod Segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6, 905–916 (2005). https://doi.org/10.1038/nrg1724

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