Development Genes and Evolution

, Volume 216, Issue 7–8, pp 395–415 | Cite as

The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence

Review

Abstract

Understanding the head is one of the great challenges in the fields of comparative anatomy, developmental biology, and palaeontology of arthropods. Numerous conflicting views and interpretations are based on an enormous variety of descriptive and experimental approaches. The interpretation of the head influences views on phylogenetic relationships within the Arthropoda as well as outgroup relationships. Here, we review current hypotheses about head segmentation and the nature of head structures from various perspectives, which we try to combine to gain a deeper understanding of the arthropod head. Though discussion about arthropod heads shows some progress, unquestioned concepts (e.g., a presegmental acron) are still a source of bias. Several interpretations are no longer tenable based on recent results from comparative molecular developmental studies, improved morphological investigations, and new fossils. Current data indicate that the anterior arthropod head comprises three elements: the protocerebral/ocular region, the deutocerebral/antennal/cheliceral segment, and the tritocerebral/pedipalpal/second antennal/intercalary segment. The labrum and the mouth are part of the protocerebral/ocular region. Whether the labrum derives from a former pair of limbs remains an open question, but a majority of data support its broad homology across the Euarthropoda. From the alignment of head segments between onychophorans and euarthropods, we develop the concept of “primary” and “secondary antennae” in Recent and fossil arthropods, posit that “primary antennae” are retained in some fossil euarthropods below the crown group level, and propose that Trilobita are stem lineage representatives of the Mandibulata.

Keywords

Segmentation Labrum Primary antennae Secondary antennae Trilobita Cambrian 

Supplementary material

References

  1. Abzhanov A, Kaufman T (2000a) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227:673–689PubMedCrossRefGoogle Scholar
  2. Abzhanov A, Kaufman T (2000b) Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 210:493–506CrossRefGoogle Scholar
  3. Abzhanov A, Kaufman T (2004) Hox genes and tagmatization of the higher Crustacea. In: Scholtz G (ed) Evolutionary developmental biology of crustacea. Balkema, Lisse, pp 43–74Google Scholar
  4. Ackermann C, Dorresteijn A, Fischer A (2005) Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J Morph 266:258–280PubMedCrossRefGoogle Scholar
  5. Aguinaldo AMA, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493PubMedCrossRefGoogle Scholar
  6. Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216(4):169–184PubMedCrossRefGoogle Scholar
  7. Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon, OxfordGoogle Scholar
  8. Angelini DR, Kaufman TC (2005) Insect appendages and comparative ontogenetics. Dev Biol 286:57–77PubMedCrossRefGoogle Scholar
  9. Arendt D, Technau U, Wittbrodt J (2001) Evolution of the bilaterian larval foregut. Nature 409:81–84PubMedCrossRefGoogle Scholar
  10. Babu KS (1965) Anatomy of the central nervous system of arachnids. Zool Jb Anat 82:1–154Google Scholar
  11. Bartolomaeus T, Purschke G, Hausen H (2005) Polychaete phylogeny based on morphological data—a comparison of current attempts. Hydrobiologia 535/536:341–356CrossRefGoogle Scholar
  12. Bateson W (1894) Materials for the study of variation. Macmillan, LondonGoogle Scholar
  13. Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Anat 86:307–458Google Scholar
  14. Bergström J, Hou X-G (2003) Arthropod origins. Bull Geosci Czech Geol Surv 78:323–334Google Scholar
  15. Bergström J, Hou X-G (2005) Early Palaeozoic non-lamellipedian arthropods. In: Koenemann S, Jenner R (eds) Crustacea and arthropod relationships. CRC, Boca Raton, pp 73–93Google Scholar
  16. Boudreaux HB (1979) Arthropod phylogeny—with special reference to insects. Wiley, New YorkGoogle Scholar
  17. Boyan GS, Williams JLD, Posser S, Bräunig P (2002) Morphological and molecular data argue for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the locust. Arthrop Struct Dev 31:65–76CrossRefGoogle Scholar
  18. Boyan GS, Bräunig P, Posser S, Williams JLD (2003) Embryonic development of the sensory innervation of the clypeo–labral complex: further support for serially homologous appendages in the locust. Arthrop Struct Dev 32:289–302CrossRefGoogle Scholar
  19. Brauer A (1895) Beiträge zur Kenntnis der Entwicklungsgeschichte des Skorpions. II. Z Wissensch Zool 59:351–433Google Scholar
  20. Briggs DEG (1976) The arthropod Branchiocaris n. gen., Middle Cambrian, Burgess Shale, British Columbia. Bull Geol Soc Canada 264:1–29Google Scholar
  21. Briggs DEG, Collins D (1999) The arthropod Alalcomenaeus cambricus Simonetta, from the Middle Cambrian Burgess Shale of British Columbia. Palaeontology 42:953–977CrossRefGoogle Scholar
  22. Brown S, Patel NH, Denell RE (1994) Embryonic expression of a single Tribolium engrailed homolog. Dev Genet 15:7–18PubMedCrossRefGoogle Scholar
  23. Browne WE, Price AL, Gerberding M, Patel NH (2005) Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149PubMedCrossRefGoogle Scholar
  24. Bruce AEE, Shankland M (1998) Expression of the head gene Lox22-Otx in the leech Helobdella and the origin of the bilaterian body plan. Dev Biol 201:101–112PubMedCrossRefGoogle Scholar
  25. Bruckmoser P (1965) Embryologische Untersuchungen über den Kopfbau der Collembole Orchesella villosa L. Zool Jb Anat 82:299–364Google Scholar
  26. Bruton DL, Whittington HB (1983) Emeraldella and Leanchoilia, two arthropods from the Burgess Shale, Middle Cambrian, British Columbia. Phil Trans R Soc Lond B 300:553–585Google Scholar
  27. Budd GE (1998) The morphology and phylogenetic significance of Kerygmachela kierkegaardi (Buen Formation, Lower Cambrian, N Greenland). Trans R Soc Edinburgh: Earth Sci 89:249–290Google Scholar
  28. Budd GE (2001) Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zool Anz 240:265–279Google Scholar
  29. Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275PubMedCrossRefGoogle Scholar
  30. Butt FH (1960) Head development in the arthropods. Biol Rev 35:43–91Google Scholar
  31. Casanova J-P (1996) Gnathophausia childressi, new species, a mysid from deep near-bottom waters off California, with remarks on the mouthparts of the genus Gnathophausia. J Crustac Biol 16:192–200CrossRefGoogle Scholar
  32. Chaudonneret J (1987) Evolution of the insect brain with special reference to the so-called tritocerebrum. In: Gupta AP (ed) Arthropod brain. Wiley, New York, pp 3–26Google Scholar
  33. Chen J, Edgecombe GD, Ramsköld L, Zhou G (1995) Head segmentation in Early Cambrian Fuxianhuia: implications for arthropod evolution. Science 268:1339–1343PubMedGoogle Scholar
  34. Chen J, Waloszek D, Maas A (2004) A new ‘great appendage’ arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 37:3–20CrossRefGoogle Scholar
  35. Chipman AD, Arthur W, Akam M (2004) Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha). Evol Dev 6:78–89PubMedCrossRefGoogle Scholar
  36. Cohen SM (1993) Imaginal disc development. In: Martinez-Arias A, Bate M (eds) Drosophila development. Cold Spring Harbor, Cold Spring Harbor, pp 747–841Google Scholar
  37. Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–272PubMedGoogle Scholar
  38. Cook CE, Smith ML, Telford MJ, Bastianello A, Akam M (2001) Hox genes and the phylogeny of arthropods. Curr Biol 11:759–763PubMedCrossRefGoogle Scholar
  39. Cotton TJ, Braddy SJ (2004) The phylogeny of arachnomorph arthropods and the origin of the Chelicerata. Trans R Soc Edinb: Earth Sci 94:169–193Google Scholar
  40. Dahl E (1956) On the differentiation of the topography of the crustacean head. Acta Zool 37:123–192CrossRefGoogle Scholar
  41. Damen WGM (2002) Parasegmental organization of spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129:1239–1250PubMedGoogle Scholar
  42. Damen WGM, Hausdorf M, Seyfarth E-A, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci U S A 95:10665–10670PubMedCrossRefGoogle Scholar
  43. Darwin C (1854) A monograph on the subclass Cirripedia, with figures of all the species. The Balanidae, the Verrucidae, etc. Ray Society, LondonGoogle Scholar
  44. Davis GK, D’Alessio JA, Patel NH (2005) Pax 3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. Dev Biol 285:169–184PubMedCrossRefGoogle Scholar
  45. de Velasco B, Mandal L, Mkrtchyan M, Hartenstein V (2006) Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev Genes Evol 216:39–51PubMedCrossRefGoogle Scholar
  46. de Rosa R, Prud’homme B, Balavoine G (2005) caudal and even-skipped in the annelid Platynereis dumerilii and the ancestry of posterior growth. Evol Dev 7:574–587PubMedCrossRefGoogle Scholar
  47. Dewel RA, Budd GE, Castano DF, Dewel WC (1999) The organization of the subesophageal nervous system in tardigrades: insights into the evolution of the arthropod hypostome and tritocerebrum. Zool Anz 238:191–203Google Scholar
  48. Dohle W (1964) Die Embryonalentwicklung von Glomeris marginata (Villers) im Vergleich zur Entwicklung anderer Diplopoden. Zool Jb Anat 81:241–310Google Scholar
  49. Dong Y, Friedrich M (2005) Comparative analysis of wingless patterning in the embryonic grasshopper. Dev Genes Evol 215:177–197PubMedCrossRefGoogle Scholar
  50. Dove H, Stollewerk A (2003) Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development 130:2161–2171PubMedCrossRefGoogle Scholar
  51. Dunlop JA, Arango CP (2004) Pycnogonid affinities: a review. J Zool Syst Evol Res 43:8–21CrossRefGoogle Scholar
  52. Edgecombe GD (2004) Morphological data, extant Myriapoda, and the myriapod stem-group. Contrib Zool 73:207–252Google Scholar
  53. Edgecombe GD, Wilson GDF, Colgan DJ, Gray MR, Cassis G (2000) Arthropod cladistics: combined analysis of histone H3 and U2 snRNA sequences and morphology. Cladistics 16:155–203CrossRefGoogle Scholar
  54. Eriksson BJ, Budd GE (2000) Onychophoran cephalic nerves and their bearing on our understanding of head segmentation and stem-group evolution of Arthropoda. Arthrop Struct Dev 29:197–209CrossRefGoogle Scholar
  55. Eriksson BJ, Tait NN, Budd GE (2003) Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J Morph 255:1–23PubMedCrossRefGoogle Scholar
  56. Fanenbruck M, Harzsch S (2005) A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthrop Struct Dev 34:343–378CrossRefGoogle Scholar
  57. Fleig R (1990) Engrailed expression and body segmentation in the honey bee Apis mellifera. Roux's Arch Dev Biol 198:467–473CrossRefGoogle Scholar
  58. Fleig R (1994) Head segmentation in the embryo of the Colorado beetle Leptinotarsa decemlineata as seen with the ant-en immunostaining. Roux's Arch Dev Biol 203:227–229CrossRefGoogle Scholar
  59. Fortey RA (2001) Trilobite systematics: the last 75 years. J Paleontol 75:1141–1151Google Scholar
  60. Fortey RA, Whittington HB (1989) The Trilobita as a natural group. Hist Biol 2:125–138Google Scholar
  61. François J (1969) Anatomie et morphologie céphalique des Protoures (Insecta Apterygota). Mém Mus Nation Hist Nat (NS) A (Zoologie) 59:1–144Google Scholar
  62. Friedrich M, Benzer S (2000) Divergent decapentaplegic expression patterns in compound eye development and the evolution of insect metamorphosis. J Exp Zool (Mol Dev Evol) 288:39–55CrossRefGoogle Scholar
  63. Gehring WJ (2004) Historical perspective on the development and evolution of eyes and photoreceptors. Int J Dev Biol 48:707–717PubMedCrossRefGoogle Scholar
  64. Giorgianni MW, Patel NH (2004) Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol Dev 6:402–410PubMedCrossRefGoogle Scholar
  65. Giribet G (2003) Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology 106:303–326PubMedCrossRefGoogle Scholar
  66. Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161PubMedCrossRefGoogle Scholar
  67. Giribet G, Richter S, Edgecombe GD, Wheeler WC (2005) The position of crustaceans within Arthropoda—evidence from nine molecular loci and morphology. In: Koenemann S, Jenner R (eds) Crustacea and arthropod relationships. CRC, Boca Raton, pp 307–352Google Scholar
  68. Goloboff PA (1993) Estimating character weights during tree search. Cladistics 9:83–91CrossRefGoogle Scholar
  69. Goodrich EJ (1897) On the relation of the arthropod head to the annelid prostomium. Q J Microsc Sci 40:259–268Google Scholar
  70. Haas MS, Brown SJ, Beeman RW (2001a) Pondering the procephalon: the segmental origin of the labrum. Dev Genes Evol 211:89–95PubMedCrossRefGoogle Scholar
  71. Haas MS, Brown SJ, Beeman RW (2001b) Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum. Dev Genes Evol 211:96–102PubMedCrossRefGoogle Scholar
  72. Haget A (1955) Expérience mettant en évidence l’origine paire du labre chez l’embryon du Coléoptère Leptinotarsa. C R Soc Biol 149:690–692Google Scholar
  73. Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin Heidelberg New YorkGoogle Scholar
  74. Harada Y, Okai N, Taguchi S, Tagawa K, Humphreys T, Satoh N (2000) Developmental expression of the hemichordate otx ortholog. Mech Dev 91:337–339PubMedCrossRefGoogle Scholar
  75. Harzsch S (2004) The tritocerebrum of Euarthropoda: a “non-drosophilocentric” perspective. Evol Dev 6:303–309PubMedCrossRefGoogle Scholar
  76. Harzsch S, Glötzner J (2002) An immunohistochemical study on structure and development of the nervous system in the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca) with remarks on the evolution of the arthropod brain. Arthrop Struct Dev 30:251–270CrossRefGoogle Scholar
  77. Harzsch S, Müller CHG, Wolf H (2005a) From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister–group relationships of Chelicerata and “Myriapoda” but favour the Mandibulata concept. Dev Genes Evol 215:53–68PubMedCrossRefGoogle Scholar
  78. Harzsch S, Wildt M, Battelle B, Waloszek D (2005b) Immunohistochemical localization of neurotransmitters in the nervous system of larval Limulus polyphemus (Chelicerata, Xiphosura): evidence for a conserved protocerebral architecture in Euarthropoda. Arthrop Struct Dev 34:327–342CrossRefGoogle Scholar
  79. Hatschek B (1878) Studien über Entwicklungsgeschichte der Anneliden. Arbeit Zool Inst Univ Wien, 57–128Google Scholar
  80. Heider K (1913) Entwicklungsgeschichte und Morphologie der Wirbellosen. In: Hinneberg P (ed) Die Kultur der Gegenwart, Teil 3, Abt. 4, Bd. 2. Teubner, Leipzig, 176–332Google Scholar
  81. Hertzel G (1984) Die Segmentation des Keimstreifens von Lithobius forficatus (L.) (Myriapoda, Chilopoda). Zool Jb Anat 112:369–386Google Scholar
  82. Heymons R (1901) Die Entwicklungsgeschichte der Scolopender. Zoologica 33:1–244Google Scholar
  83. Hirth F, Therianos S, Loop T, Gehring WJ, Reichert H, Furukubo-Tokunaga K (1995) Developmental defects in brain segmentation caused by mutations of the homeobox genes orthodenticle and empty spiracles in Drosophila. Neuron 15:769–778PubMedCrossRefGoogle Scholar
  84. Holmgren N (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Vet Akad Handl Stockholm 56:1–303Google Scholar
  85. Hou X-G (1999) New rare bivalved arthropods from the Lower Cambrian Chengjiang fauna, Yunnan, China. J Paleontol 73:102–116Google Scholar
  86. Hou X-G, Bergström J (1997) Arthropods of the Lower Cambrian Chengjiang fauna, southwest China. Fossils Strata 45:1–116Google Scholar
  87. Hou X-G, Aldridge RJ, Bergström J, Siveter DJ, Siveter DJ, Feng X-H (2004) The Cambrian Fossils of Chengjiang, China. The flowering of early animal life. Blackwell, OxfordGoogle Scholar
  88. Hughes CL, Kaufman TC (2002) Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol 246:47–61CrossRefGoogle Scholar
  89. Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157PubMedCrossRefGoogle Scholar
  90. Inoue Y, Niwa N, Mito T, Ohuchi H, Yoshika H, Noji S (2002) Expression patterns of hedgehog, wingless, and decapentaplegic during gut formation of Gryllus bimaculatus (cricket). Mech Dev 110:245–248PubMedCrossRefGoogle Scholar
  91. Jager M, Murienne J, Clabaut C, Deutsch J, Le Guyader H, Manuel M (2006) Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider. Nature 411:506–508CrossRefGoogle Scholar
  92. Janetschek H (1970) 3. Protura (Beintastler) In: Helmcke J-G, Starck D, Wermuth H (eds) Handbuch der Zoologie, IV. Band: Arthropoda-2. Hälfte: Insecta, 2. Teil: Spezielles. Parey, Berlin, pp 1–72Google Scholar
  93. Janssen R, Prpic N-M, Damen WGM (2004) Gene expression suggests decoupled dorsal and ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Dev Biol 268:89–104PubMedCrossRefGoogle Scholar
  94. Jenner RA, Scholtz G (2005) Playing another round of metazoan phylogenetics: historical epistemology, sensitivity analysis, and the position of Arthropoda within the Metazoa on the basis of morphology. In: Koenemann S, Jenner R (eds) Crustacea and Arthropod relationships. CRC, Boca Raton, pp 355–385Google Scholar
  95. Jockusch EL, Ober KA (2004) Hypothesis testing in evolutionary developmental biology: a case study from insect wings. J Heredity 95:382–396CrossRefGoogle Scholar
  96. Kadner D, Stollewerk A (2004) Neurogenesis in the chilopod Lithobius forficatus suggests more similarities to chelicerates than to insects. Dev Genes Evol 214:367–379PubMedCrossRefGoogle Scholar
  97. Kjellsvig-Waering EN (1986) A restudy of the fossil Scorpionida of the world. Palaeontogr Am 55:1–287Google Scholar
  98. Kuratani S (2003) Evolutionary developmental biology and vertebrate head segmentation: a perspective from developmental constraint. Theory Biosci 122:230–251CrossRefGoogle Scholar
  99. Kusche K, Hembach A, Hagner-Holler S, Genauer W, Burmester T (2003) Complete subunit sequences, structure and evolution of the 6×6-mer hemocyanin from the common house centipede, Scutigera coleoptrata. Eur J Biochem 270:2860–2868PubMedCrossRefGoogle Scholar
  100. Lauterbach K-E (1973) Schlüsselereignisse in der Evolution der Stammgruppe der Euarthropoda. Zool Beitr (NF) 19:251–299Google Scholar
  101. Lauterbach K-E (1980a) Schlüsselereignisse in der Evolution des Grundplans der Mandibulata (Arthropoda). Abh Naturwiss Ver Hamburg NF 23:105–161Google Scholar
  102. Lauterbach K-E (1980b) Schlüsselereignisse in der Evolution des Grundplans der Arachnata (Arthropoda). Abh Naturwiss Ver Hamburg NF 23:163–327Google Scholar
  103. Li Y, Brown SJ, Hausdorf B, Tautz D, Denell RE, Finkelstein R (1996) Two orthodenticle-related genes in the short-germ beetle Tribolium castaneum. Dev Genes Evol 206:35–45CrossRefGoogle Scholar
  104. Maas A, Waloszek D (2001) Cambrian derivatives of the early arthropod stem lineage, pentastomids, tardigrades and lobopodians—an ‘Orsten’ perspective. Zool Anz 240:451–459Google Scholar
  105. Maas A, Waloszek D, Chen J, Braun A, Wang X, Huang D (2004) Phylogeny and life habits of early arthropods—predation in the Early Cambrian sea. Prog Nat Sci 14:158–166CrossRefGoogle Scholar
  106. Mallatt JM, Garey JR, Shultz JW (2004) Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol 31:178–191PubMedCrossRefGoogle Scholar
  107. Manton SM (1928) On the embryology of the crustacean Nebalia bipes. Phil Trans R Soc Lond B 223:163–238Google Scholar
  108. Manton SM (1949) Studies on the Onychophora VII. The early embryonic stages of Peripatopsis and some general considerations concerning the morphology and phylogeny of the Arthropoda. Phil Trans R Soc B 233:483–580Google Scholar
  109. Manzanares M, Williams TA, Marco R, Garesse R (1996) Segmentation in the crustacean Artemia: engrailed staining studied with an antibody raised against the Artemia protein. Roux's Arch Dev Biol 205:424–431CrossRefGoogle Scholar
  110. Maxmen A, Browne WE, Martindale MQ, Giribet G (2005) Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment. Nature 437:1144–1148PubMedCrossRefGoogle Scholar
  111. Mayer G, Koch M (2005) Ultrastructure and fate of the nephridial anlagen in the antennal segment of Epiperipatus biolleyi (Onychophora, Peripatidae) evidence for the onychophoran antennae being modified legs. Arthrop Struct Dev 34:471–480CrossRefGoogle Scholar
  112. Meisenheimer J (1902) Beiträge zur Entwicklungsgeschichte der Pantopoden. I. Die Entwicklung von Ammothea echinata Hodge bis zur Ausbildung derLarvenform. Zeitschr Wiss Zool 72:191–248Google Scholar
  113. Minelli A (2003) The origin and evolution of appendages. Int J Dev Biol 47:573–581PubMedGoogle Scholar
  114. Minelli A, Fusco G (2004) Evo–devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429PubMedCrossRefGoogle Scholar
  115. Mittmann B, Scholtz G (2001) Distal-less expression in embryos of Limulus polyphemus (Chelicerata, Xiphosura) and Lepisma saccharina (Insecta, Zygentoma) suggests as role in the development of mechanoreceptors, chemoreceptors, and the CNS. Dev Genes Evol 211:232–243PubMedCrossRefGoogle Scholar
  116. Mittmann B, Scholtz G (2003) Development of the nervous system in the “head” of Limulus polyphemus (Chelicerata, Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev Genes Evol 213:9–17PubMedGoogle Scholar
  117. Müller KJ, Walossek D (1986) Martinssonia elongata gen. et sp.n., a crustacean-like euarthropod from the Upper Cambrian ‘Orsten’ of Sweden. Zool Scr 15:73–92CrossRefGoogle Scholar
  118. Nederbragt AJ, te Welscher, P, van den Driesche S, van Loon A, Dictus WJAG (2002) Novel and conserved roles for orthodenticle/otx and orthopedia/otp orthologs in the gastropod mollusc Patella vulgata. Dev Genes Evol 212:330–337PubMedCrossRefGoogle Scholar
  119. Negrisolo E, Minelli A, Valle G (2004) The mitochondrial genome of the house centipede Scutigera and the monophyly versus paraphyly of myriapods. Mol Bio Evol 21:770–780CrossRefGoogle Scholar
  120. Nielsen C (2001) Animal evolution. Interrelationships of the living phyla, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  121. Nielsen C (2005a) Trochophora larvae and adult body regions in annelids: some conclusions. Hydrobiologia 535/536:23–24CrossRefGoogle Scholar
  122. Nielsen C (2005b) Larval and adult brains. Evol Dev 7:483–489PubMedCrossRefGoogle Scholar
  123. Niwa N, Saitoh M, Ohuchi H, Yoshioka H, Noji S (1997) Correlation between Distal-less expression patterns and structures of appendages in development of the two-spotted cricket, Gryllus bimaculatus. Zool Sci 14:115–125CrossRefGoogle Scholar
  124. Northcutt RG (2005) The new head hypothesis revisited. J Exp Zool (Mol Dev Evol) 304B:274–297CrossRefGoogle Scholar
  125. Nulsen C, Nagy LM (1999) The role of wingless in the development of multibranched crustacean limbs. Dev Genes Evol 209:340–348PubMedCrossRefGoogle Scholar
  126. Oishi S (1959) Studies on the teloblasts in the decapod embryo I. Origin of teloblasts in Heptacarpus rectirostris (Stimpson). Embryol 4:283–309CrossRefGoogle Scholar
  127. Olesen J (2004) On the ontogeny of the Branchiopoda (Crustacea): contribution of development to phylogeny and classification. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Balkema, Lisse, pp 217–269Google Scholar
  128. Olesen J, Richter S, Scholtz G (2001) The evolutionary transformation of phyllopodous to stenopodous limbs in the Branchiopoda (Crustacea)—is there a common mechanism for early limb development in arthropods? Int J Dev Biol 45:869–876PubMedGoogle Scholar
  129. Olsson L, Ericsson, R, Cerny R (2005) Vertebrate head development: segmentation, novelties, and homology. Theory Biosci 124:145–163CrossRefPubMedGoogle Scholar
  130. Osborne PW, Dearden PK (2005) Expression of Pax group III genes in the honey bee (Apis mellifera). Dev Genes Evol 215:499–508PubMedCrossRefGoogle Scholar
  131. Page DT (2004) A mode of arthropod brain evolution suggested by Drosophila commissure development. Evol Dev 6:25–31PubMedCrossRefGoogle Scholar
  132. Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363–1366PubMedGoogle Scholar
  133. Patel NH, Kornberg TB, Goodman CS (1989) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212PubMedGoogle Scholar
  134. Paulus H, Weygoldt P (1996) Artrhropoda, Gliederfüßer. In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer, Stuttgart, pp 411–419Google Scholar
  135. Peterson MD, Popadic A, Kaufman TC (1998) The expression of two engrailed-related genes in an apterygote insect and a phylogenetic analysis of insect engrailed-related genes. Dev Genes Evol 208:547–557PubMedCrossRefGoogle Scholar
  136. Pflugfelder O (1948) Entwicklung von Paraperipatus anboinensis n. sp. Zool Jb Anat 69:443–492Google Scholar
  137. Pisani D, Poling LL, Lyons-Weiler M, Hedges SB (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol 2:1–10PubMedCrossRefGoogle Scholar
  138. Popadic A, Panganiban G, Rusch D, Shear WA, Kaufman TC (1998) Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev Genes Evol 208:142–150PubMedCrossRefGoogle Scholar
  139. Pross A (1966) Untersuchungen zur Entwicklungsgeschichte der Araneae (Pardosa hortensis (Thorell)) unter besonderer Berücksichtigung des vorderen Prosomaabschnitts. Z Morph Ökol Tiere 58:38–108CrossRefGoogle Scholar
  140. Prpic N-M, Tautz D (2003) The expression of the proximodistal axis patterning genes Distal-less and dachshund in the appendages of Glomeris marginata (Myriapoda: Diplopoda) suggests a special role of these genes in patterning the head appendages. Dev Biol 260:97–112PubMedCrossRefGoogle Scholar
  141. Prpic N-M, Wigand B, Damen WGM, Klingler M (2001) Expression of dachshund in wild-type and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Dev Genes Evol 211:467–477PubMedCrossRefGoogle Scholar
  142. Prpic N-M, Janssen R, Wigand B, Klingler M, Damen WGM (2003) Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signaling. Dev Biol 265:119–140CrossRefGoogle Scholar
  143. Prud’homme B, de Rosa R, Arendt D, Julien J-F, Pajaziti R, Dorresteijn AWC, Adoutte A, Wittbrodt J, Balavoine G (2003) Arthropod-like expression patterns of engrailed and wingless in the annelid Platynereis dumerilii suggest a role in segment formation. Curr Biol 13:1876–1881PubMedCrossRefGoogle Scholar
  144. Pultz MA, Pitt JN, Alto NM (1999) Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis. Development 126:701–710PubMedGoogle Scholar
  145. Pultz MA, Westendorf L, Gale SD, Hawkins K, Lynch J, Pitt JN, Reeves NL, Yao JCY, Small S, Desplan C, Leaf DS (2005) A major role for zygotic hunchback in patterning the Nasonia embryo. Development 132:3705–3715PubMedCrossRefGoogle Scholar
  146. Ramsköld L, Edgecombe GD (1991) Trilobite monophyly revisited. Hist Biol 4:267–283CrossRefGoogle Scholar
  147. Rempel JG (1975) The evolution of the insect head: the endless dispute. Quaest Ent 11:7–25Google Scholar
  148. Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136CrossRefGoogle Scholar
  149. Richter S, Wirkner C (2004) Kontroversen in der phylogenetischen Systematik der Euarthropoda. Sber Ges Naturf Freunde Berlin (NF) 43:73–102Google Scholar
  150. Rogers BT, Kaufman TC (1997) Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. Int Rev Cytol 174:1–84PubMedCrossRefGoogle Scholar
  151. Rogers BT, Peterson MD, Kaufman TC (2002) The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes. Evol Dev 4:96–110PubMedCrossRefGoogle Scholar
  152. Rohrschneider I (1968) Beiträge zur Entwicklung des Vorderkopfes und der Mundregion von Periplaneta americana. Zool Jb Anat 85:537–578Google Scholar
  153. Sanchez-Salazar J, Pletcher MT, Bennett RL, Brown SJ, Dandamundi TJ, Denell RE, Doctor JS (1996) The Tribolium decapentaplagic gene is similar in sequence, structure, and expression to the Drosophila dpp gene. Dev Genes Evol 206:237–246CrossRefGoogle Scholar
  154. Schmidt-Ott U, Technau GM (1992) Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 116:111–125PubMedGoogle Scholar
  155. Schmidt-Ott U, Sander K, Technau GM (1994a) Expression of engrailed in embryos of a beetle and five dipteran species with special reference to the terminal regions. Roux Arch Dev Biol 203:298–303CrossRefGoogle Scholar
  156. Schmidt-Ott U, González-Gaitán M, Jäckle H, Technau GM (1994b) Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants. Proc Natl Acad Sci U S A 91:8363–8367PubMedCrossRefGoogle Scholar
  157. Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR (1998) The position of the Arthropoda in the phylogenetic system. J Morphol 238:263–285CrossRefGoogle Scholar
  158. Schneuwly S, Klemenz R, Gehring WJ (1987) Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia. Nature 325:816–818PubMedCrossRefGoogle Scholar
  159. Scholl G (1963) Embryologische Untersuchungen an Tanaidaceen (Heterotanais oerstedi Kröyer). Zool Jb Anat 80:500–554Google Scholar
  160. Scholl G (1969) Die Embryonalentwicklung des Kopfes und Prothorax von Carausius morosus Br. (Insecta, Phasmida). Z Morph Tiere 65:1–142CrossRefGoogle Scholar
  161. Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154CrossRefGoogle Scholar
  162. Scholtz G (1995) Head segmentation in Crustacea—an immunocytochemical study. Zoology 98:104–114Google Scholar
  163. Scholtz G (1997) Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman and Hall, London, pp 317–332Google Scholar
  164. Scholtz G (2001) Evolution of developmental patterns in arthropods-the contribution of gene expression to morphology and phylogenetics. Zoology 103:99–111Google Scholar
  165. Scholtz G (2002) The Articulata hypothesis—or what is a segment? Organ Divers Evol 2:197–215CrossRefGoogle Scholar
  166. Scholtz G (2003) Is the taxon Articulata obsolete? Arguments in favour of a close relationship between annelids and arthropods. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) Proceedings of the 18th International Congress of Zoology, Athens 2000. Penfolds, Sofia, pp 489–501Google Scholar
  167. Scholtz G (2004) Baupläne versus ground patterns, phyla versus monophyla: aspects of patterns and processes in evolutionary developmental biology. In: Scholtz G (ed) Evolutionary developmental biology of Crustacea. Balkema, Lisse, pp 3–16Google Scholar
  168. Scholtz G (2005) Homology and ontogeny: pattern and process in comparative developmental biology. Theory Biosci 124:121–143CrossRefPubMedGoogle Scholar
  169. Scholtz G, Edgecombe GD (2005) Heads, Hox and the phylogenetic position of trilobites. In: Koenemann S, Jenner R (eds) Crustacea and arthropod relationships. CRC, Boca Raton, pp 139–165Google Scholar
  170. Scholtz G, Patel NH, Dohle W (1994) Serially homologous engrailed stripes are generated via different cell lineages in the germ band of amphipod crustaceans (Malacostraca, Peracarida). Int J Dev Biol 38:471–478PubMedGoogle Scholar
  171. Scholtz G, Mittman B, Gerberding M (1998) The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42:801–810PubMedGoogle Scholar
  172. Schoppmeier M, Damen WGM (2001) Double-stranded RNA interference in the spider Cupiennius salei: the role of Distal-less is evolutionarily conserved in arthropod appendage formation. Dev Genes Evol 211:76–82PubMedCrossRefGoogle Scholar
  173. Schröder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621–625PubMedCrossRefGoogle Scholar
  174. Seaver EC (2003) Segmentation: mono or polyphyletic? Int J Dev Biol 47:583–595PubMedGoogle Scholar
  175. Seaver EC, Kaneshige LM (2006) Expression of “segmentation” genes during larval and juvenile development in the polychaetes Capitella sp. I and H. elegans. Dev Biol 289:179–194PubMedCrossRefGoogle Scholar
  176. Seaver EC, Thamm K, Hill SD (2005) Growth patterns during segmentation in the two polychaete annelids, Capitella sp. I and Hydroides elegans: comparisons at distinct life history stages. Evol Dev 7:312–326PubMedCrossRefGoogle Scholar
  177. Selden PA (1981) Functional morphology of the prosoma of Baltoeurypterus tetragonophthalmus (Fischer) (Chelicerata: Eurypterida). Trans R Soc Edinburgh: Earth Sci 72:9–48Google Scholar
  178. Semmler H (2005) Immuncytochemische Studien zur larvalen Myo- und Neuroanatomie von Balanus improvisus (Crustacea, Cirripedia, Thecostraca). Diplom Thesis: Humboldt-Universität zu BerlinGoogle Scholar
  179. Shiga Y, Yasumoto R, Yamagata H, Hayashi S (2002) Evolving role of Antennapedia protein in arthropod limb patterning. Development 129:3555–3561PubMedGoogle Scholar
  180. Siewing R (1963) Das Problem der Arthropodenkopfsegmentierung. Zool Anz 170:429–468Google Scholar
  181. Siewing R (1969) Lehrbuch der vergleichenden Entwicklungsgeschichte der Tiere. Parey, HamburgGoogle Scholar
  182. Simonnet F, Deutsch J, Quéinnec E (2004) hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev Genes Evol 214:527–545CrossRefGoogle Scholar
  183. Snodgrass RE (1960) Facts and theories concerning the insect head. Smithson Misc Collect 142:1–61Google Scholar
  184. Starck D (1963) Die Metamerie des Kopfes der Wirbeltiere. Zool Anz 170:393–428Google Scholar
  185. Stein M, Waloszek D, Maas A (2005) Oelandicaris oelandica and the stem lineage of Crustacea. In: Koenemann S, Jenner R (eds) Crustacea and arthropod relationships. CRC, Boca Raton, pp 55–71Google Scholar
  186. Størmer L (1944) On the relationships and phylogeny of fossil and recent Arachnomorpha. Skrift Utgitt Norske Vidensk-akad Oslo I Math-Naturvitensk Klasse 5:1–158Google Scholar
  187. Tamarelle M (1984) Transient rudiments of second antennae on the “intercalary” segment of embryos of Anurida maritima Guer. (Collembola: Arthropleona) and Hyphantria cunea Drury (Lepidoptera: Arctiidae) Int J Insect Morphol Embryol 13:331–336CrossRefGoogle Scholar
  188. Tautz D (2004) Segmentation. Dev Cell 7:301–312PubMedCrossRefGoogle Scholar
  189. Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci U S A 95:10671–10675PubMedCrossRefGoogle Scholar
  190. Thomas RH, Telford MJ (1999) Appendage development in embryos of the oribatid mite Archegozetes longisetus (Acari, Oribatei, Thrypochthoniidae) Acta Zool 80:193–200CrossRefGoogle Scholar
  191. Tiegs OW (1940) The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q J Microsc Sci 82:1–225Google Scholar
  192. Tomsa JM, Langeland JA (1999) Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol 207:26–37PubMedCrossRefGoogle Scholar
  193. Ullmann SL (1964) The origin and structure of the mesoderm and the formation of the coelomic sacs in Tenebrio molitor L (Insecta, Coleoptera). Phil Trans R Soc Lond B 747:245–276Google Scholar
  194. Umesono Y, Watanabe K, Agata K (1999) Distinct structural domains in the planarian brain defined by the expression of evolutionarily conserved homeobox genes. Dev Genes Evol 209:31–39PubMedCrossRefGoogle Scholar
  195. Ungerer P, Wolff C (2005) External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89–99CrossRefGoogle Scholar
  196. Urbach R, Technau G (2003a) Early steps in building the insect brain: neuroblasts formation and segmental patterning in the developing brain of different insect species. Arthrop Struct Dev 32:103–123CrossRefGoogle Scholar
  197. Urbach R, Technau G (2003b) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130:3621–3637PubMedCrossRefGoogle Scholar
  198. Urbach R, Technau G, Breidbach O (2003) Spatial and temporal pattern of neuroblasts, proliferation, and engrailed expression during early brain development. Arthrop Struct Dev 32:125–140CrossRefGoogle Scholar
  199. Vilpoux K, Waloszek D (2003) Larval development and morphogenesis of the sea spider Pycnogonum litorale (Ström, 1762) and the tagmosis of the body of Pantopoda. Arthrop Struct Dev 32:349–383CrossRefGoogle Scholar
  200. von Wistinghausen C (1891) Untersuchungen über die Entwicklung von Nereis dumerilii. Mitt Zool Stat Neapel 10:41–74Google Scholar
  201. Wada S (1965) Analyse der Kopf-Hals-Region von Tachycines (Saltatoria) in morphogenetische Einheiten. II. Mitteilung: Experimentell-teratologische Befunde am Kopfskelett mit Berücksichtigung des zentralen Nervensystems. Zool Jb Anat 83:235–326Google Scholar
  202. Wägele J-W, Misof B (2001) On the quality of evidence in phylogeny reconstruction: a reply to Zrzavý’s defence of the ‘Ecdysozoa’ hypothesis. J Zool Syst Evol Res 39:165–176CrossRefGoogle Scholar
  203. Walossek D (1993) The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32:3–202Google Scholar
  204. Waloszek D (2003) Cambrian ‘Orsten’-type preserved arthropods and the phylogeny of Crustacea. In: Legakis A, Sfenthourakis, S, Polymeni R and Thessalou-Legaki M (eds) Proceedings of the 18th International Congress of Zoology, Athens 2000:69–87Google Scholar
  205. Waloszek D, Dunlop JA (2002) A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian ‘Orsten’ of Sweden, and the phylogenetic position of pycnogonids. Palaeontology 45:421–446CrossRefGoogle Scholar
  206. Walossek D, Müller KJ (1990) Upper Cambrian stem-lineage crustaceans and their bearing upon the monophyletic origin of Crustacea and the position of Agnostus. Lethaia 23:409–427Google Scholar
  207. Waloszek D, Chen J, Maas A, Wang X (2005) Early Cambrian arthropods—new insights into arthropod head and structural evolution. Arthrop Struct Dev 34:189–205CrossRefGoogle Scholar
  208. Weber H (1952) Morphologie, Histologie und Entwicklungsgeschichte der Articulaten II. Die Kopfsegmentierung und die Morphologie des Kopfes überhaupt. Fortschr Zool 9:18–231Google Scholar
  209. Weygoldt P (1985) Ontogeny of the arachnid central nervous system. In: Barth FG (ed) Neurobiology of arachnids. Springer, Berlin Heidelberg New York, pp 20–37Google Scholar
  210. Whittington HB (1975) Trilobites with appendages from the Middle Cambrian Burgess Shale, British Columbia. Fossils Strata 4:97–136Google Scholar
  211. Whittington HB (1980) Exoskeleton, moult stage, appendage morphology and habits of the Middle Cambrian trilobite Olenoides serratus. Palaeontology 23:171–204Google Scholar
  212. Winter G (1980) Beiträge zur Morphologie und Embryologie des vorderen Körperabschnitts (Cephalosoma) der Pantopoda Gerstaecker, 1863. Z Zoolog Syst Evol Forsch 18:27–61Google Scholar
  213. Wolff C (2004) Die Beinentwicklung des amphipoden Krebses Orchestia cavimana (Peracarida, Malacostraca - eine zellgenealogische Studie. Doctoral Thesis, Humboldt-Universität zu BerlinGoogle Scholar
  214. Woltereck R (1905) Zur Kopffrage der Anneliden. Verh Dtsch Zool Ges 15:154–186Google Scholar
  215. Yamamoto DS, Sumitani M, Tojo K, Lee JM, Hatakeyama M (2004) Cloning of a decapentaplegic orthologue from the sawfly, Athalia rosae (Hymenoptera) and its expression in the embryonic appendages. Dev Genes Evol 214:128–133PubMedCrossRefGoogle Scholar
  216. Younossi-Hartenstein A, Green P, Liaw G-J, Rudolph K, Lengyel J, Hartenstein V (1997) Control of early neurogenesis of the Drosophila brain by the head gap genes tll, otd, ems, and btd. Dev Biol 182:270–283PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Humboldt-Universität zu BerlinInstitut für Biologie/Vergleichende ZoologieBerlinGermany
  2. 2.Australian MuseumSydneyAustralia

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