Skip to main content
Log in

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

  • Review
  • Published:
Development Genes and Evolution Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abzhanov A, Kaufman T (2000a) Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev Biol 227:673–689

    Article  PubMed  CAS  Google Scholar 

  • Abzhanov A, Kaufman T (2000b) Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 210:493–506

    Article  CAS  Google Scholar 

  • 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 43–74

    Google Scholar 

  • Ackermann C, Dorresteijn A, Fischer A (2005) Clonal domains in postlarval Platynereis dumerilii (Annelida: Polychaeta). J Morph 266:258–280

    Article  PubMed  Google Scholar 

  • 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 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216(4):169–184

    Article  PubMed  Google Scholar 

  • Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon, Oxford

    Google Scholar 

  • Angelini DR, Kaufman TC (2005) Insect appendages and comparative ontogenetics. Dev Biol 286:57–77

    Article  PubMed  CAS  Google Scholar 

  • Arendt D, Technau U, Wittbrodt J (2001) Evolution of the bilaterian larval foregut. Nature 409:81–84

    Article  PubMed  CAS  Google Scholar 

  • Babu KS (1965) Anatomy of the central nervous system of arachnids. Zool Jb Anat 82:1–154

    Google Scholar 

  • Bartolomaeus T, Purschke G, Hausen H (2005) Polychaete phylogeny based on morphological data—a comparison of current attempts. Hydrobiologia 535/536:341–356

    Article  Google Scholar 

  • Bateson W (1894) Materials for the study of variation. Macmillan, London

    Google Scholar 

  • Benesch R (1969) Zur Ontogenie und Morphologie von Artemia salina L. Zool Jb Anat 86:307–458

    Google Scholar 

  • Bergström J, Hou X-G (2003) Arthropod origins. Bull Geosci Czech Geol Surv 78:323–334

    Google Scholar 

  • 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 73–93

    Google Scholar 

  • Boudreaux HB (1979) Arthropod phylogeny—with special reference to insects. Wiley, New York

    Google Scholar 

  • 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 31:65–76

    Article  CAS  Google Scholar 

  • 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 32:289–302

    Article  CAS  Google Scholar 

  • Brauer A (1895) Beiträge zur Kenntnis der Entwicklungsgeschichte des Skorpions. II. Z Wissensch Zool 59:351–433

    Google Scholar 

  • Briggs DEG (1976) The arthropod Branchiocaris n. gen., Middle Cambrian, Burgess Shale, British Columbia. Bull Geol Soc Canada 264:1–29

    Google Scholar 

  • Briggs DEG, Collins D (1999) The arthropod Alalcomenaeus cambricus Simonetta, from the Middle Cambrian Burgess Shale of British Columbia. Palaeontology 42:953–977

    Article  Google Scholar 

  • Brown S, Patel NH, Denell RE (1994) Embryonic expression of a single Tribolium engrailed homolog. Dev Genet 15:7–18

    Article  PubMed  CAS  Google Scholar 

  • Browne WE, Price AL, Gerberding M, Patel NH (2005) Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149

    Article  PubMed  Google Scholar 

  • 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 201:101–112

    Article  PubMed  CAS  Google Scholar 

  • Bruckmoser P (1965) Embryologische Untersuchungen über den Kopfbau der Collembole Orchesella villosa L. Zool Jb Anat 82:299–364

    Google Scholar 

  • Bruton DL, Whittington HB (1983) Emeraldella and Leanchoilia, two arthropods from the Burgess Shale, Middle Cambrian, British Columbia. Phil Trans R Soc Lond B 300:553–585

    Google Scholar 

  • Budd GE (1998) The morphology and phylogenetic significance of Kerygmachela kierkegaardi (Buen Formation, Lower Cambrian, N Greenland). Trans R Soc Edinburgh: Earth Sci 89:249–290

    Google Scholar 

  • Budd GE (2001) Tardigrades as ‘stem-group arthropods’: the evidence from the Cambrian fauna. Zool Anz 240:265–279

    Google Scholar 

  • Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275

    Article  PubMed  CAS  Google Scholar 

  • Butt FH (1960) Head development in the arthropods. Biol Rev 35:43–91

    Google Scholar 

  • 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 16:192–200

    Article  Google Scholar 

  • 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 3–26

    Google Scholar 

  • Chen J, Edgecombe GD, Ramsköld L, Zhou G (1995) Head segmentation in Early Cambrian Fuxianhuia: implications for arthropod evolution. Science 268:1339–1343

    CAS  PubMed  Google Scholar 

  • 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 37:3–20

    Article  Google Scholar 

  • Chipman AD, Arthur W, Akam M (2004) Early development and segment formation in the centipede, Strigamia maritima (Geophilomorpha). Evol Dev 6:78–89

    Article  PubMed  Google Scholar 

  • Cohen SM (1993) Imaginal disc development. In: Martinez-Arias A, Bate M (eds) Drosophila development. Cold Spring Harbor, Cold Spring Harbor, pp 747–841

    Google Scholar 

  • Cohen S, Jürgens G (1991) Drosophila headlines. Trends Genet 7:267–272

    PubMed  CAS  Google Scholar 

  • Cook CE, Smith ML, Telford MJ, Bastianello A, Akam M (2001) Hox genes and the phylogeny of arthropods. Curr Biol 11:759–763

    Article  PubMed  CAS  Google Scholar 

  • Cotton TJ, Braddy SJ (2004) The phylogeny of arachnomorph arthropods and the origin of the Chelicerata. Trans R Soc Edinb: Earth Sci 94:169–193

    Google Scholar 

  • Dahl E (1956) On the differentiation of the topography of the crustacean head. Acta Zool 37:123–192

    Article  Google Scholar 

  • Damen WGM (2002) Parasegmental organization of spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129:1239–1250

    PubMed  CAS  Google Scholar 

  • 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 95:10665–10670

    Article  PubMed  CAS  Google Scholar 

  • Darwin C (1854) A monograph on the subclass Cirripedia, with figures of all the species. The Balanidae, the Verrucidae, etc. Ray Society, London

  • Davis GK, D’Alessio JA, Patel NH (2005) Pax 3/7 genes reveal conservation and divergence in the arthropod segmentation hierarchy. Dev Biol 285:169–184

    Article  PubMed  CAS  Google Scholar 

  • de Velasco B, Mandal L, Mkrtchyan M, Hartenstein V (2006) Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev Genes Evol 216:39–51

    Article  PubMed  Google Scholar 

  • 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 7:574–587

    Article  PubMed  Google Scholar 

  • 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 238:191–203

    Google Scholar 

  • Dohle W (1964) Die Embryonalentwicklung von Glomeris marginata (Villers) im Vergleich zur Entwicklung anderer Diplopoden. Zool Jb Anat 81:241–310

    Google Scholar 

  • Dong Y, Friedrich M (2005) Comparative analysis of wingless patterning in the embryonic grasshopper. Dev Genes Evol 215:177–197

    Article  PubMed  CAS  Google Scholar 

  • Dove H, Stollewerk A (2003) Comparative analysis of neurogenesis in the myriapod Glomeris marginata (Diplopoda) suggests more similarities to chelicerates than to insects. Development 130:2161–2171

    Article  PubMed  CAS  Google Scholar 

  • Dunlop JA, Arango CP (2004) Pycnogonid affinities: a review. J Zool Syst Evol Res 43:8–21

    Article  Google Scholar 

  • Edgecombe GD (2004) Morphological data, extant Myriapoda, and the myriapod stem-group. Contrib Zool 73:207–252

    Google Scholar 

  • 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 16:155–203

    Article  Google Scholar 

  • 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 29:197–209

    Article  CAS  Google Scholar 

  • Eriksson BJ, Tait NN, Budd GE (2003) Head development in the onychophoran Euperipatoides kanangrensis with particular reference to the central nervous system. J Morph 255:1–23

    Article  PubMed  Google Scholar 

  • 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 34:343–378

    Article  Google Scholar 

  • Fleig R (1990) Engrailed expression and body segmentation in the honey bee Apis mellifera. Roux's Arch Dev Biol 198:467–473

    Article  Google Scholar 

  • 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 203:227–229

    Article  Google Scholar 

  • Fortey RA (2001) Trilobite systematics: the last 75 years. J Paleontol 75:1141–1151

    Google Scholar 

  • Fortey RA, Whittington HB (1989) The Trilobita as a natural group. Hist Biol 2:125–138

    Google Scholar 

  • François J (1969) Anatomie et morphologie céphalique des Protoures (Insecta Apterygota). Mém Mus Nation Hist Nat (NS) A (Zoologie) 59:1–144

    Google Scholar 

  • 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) 288:39–55

    Article  CAS  Google Scholar 

  • Gehring WJ (2004) Historical perspective on the development and evolution of eyes and photoreceptors. Int J Dev Biol 48:707–717

    Article  PubMed  Google Scholar 

  • Giorgianni MW, Patel NH (2004) Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol Dev 6:402–410

    Article  PubMed  Google Scholar 

  • Giribet G (2003) Molecules, development and fossils in the study of metazoan evolution; Articulata versus Ecdysozoa revisited. Zoology 106:303–326

    Article  PubMed  CAS  Google Scholar 

  • Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161

    Article  PubMed  CAS  Google Scholar 

  • 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 307–352

    Google Scholar 

  • Goloboff PA (1993) Estimating character weights during tree search. Cladistics 9:83–91

    Article  Google Scholar 

  • Goodrich EJ (1897) On the relation of the arthropod head to the annelid prostomium. Q J Microsc Sci 40:259–268

    Google Scholar 

  • Haas MS, Brown SJ, Beeman RW (2001a) Pondering the procephalon: the segmental origin of the labrum. Dev Genes Evol 211:89–95

    Article  PubMed  CAS  Google Scholar 

  • Haas MS, Brown SJ, Beeman RW (2001b) Homeotic evidence for the appendicular origin of the labrum in Tribolium castaneum. Dev Genes Evol 211:96–102

    Article  PubMed  CAS  Google Scholar 

  • Haget A (1955) Expérience mettant en évidence l’origine paire du labre chez l’embryon du Coléoptère Leptinotarsa. C R Soc Biol 149:690–692

    CAS  Google Scholar 

  • Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Harada Y, Okai N, Taguchi S, Tagawa K, Humphreys T, Satoh N (2000) Developmental expression of the hemichordate otx ortholog. Mech Dev 91:337–339

    Article  PubMed  CAS  Google Scholar 

  • Harzsch S (2004) The tritocerebrum of Euarthropoda: a “non-drosophilocentric” perspective. Evol Dev 6:303–309

    Article  PubMed  Google Scholar 

  • 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 30:251–270

    Article  Google Scholar 

  • 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 215:53–68

    Article  PubMed  Google Scholar 

  • 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 34:327–342

    Article  CAS  Google Scholar 

  • Hatschek B (1878) Studien über Entwicklungsgeschichte der Anneliden. Arbeit Zool Inst Univ Wien, 57–128

  • Heider K (1913) Entwicklungsgeschichte und Morphologie der Wirbellosen. In: Hinneberg P (ed) Die Kultur der Gegenwart, Teil 3, Abt. 4, Bd. 2. Teubner, Leipzig, 176–332

  • Hertzel G (1984) Die Segmentation des Keimstreifens von Lithobius forficatus (L.) (Myriapoda, Chilopoda). Zool Jb Anat 112:369–386

    Google Scholar 

  • Heymons R (1901) Die Entwicklungsgeschichte der Scolopender. Zoologica 33:1–244

    Google Scholar 

  • 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 15:769–778

    Article  PubMed  CAS  Google Scholar 

  • Holmgren N (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Vet Akad Handl Stockholm 56:1–303

    Google Scholar 

  • Hou X-G (1999) New rare bivalved arthropods from the Lower Cambrian Chengjiang fauna, Yunnan, China. J Paleontol 73:102–116

    Google Scholar 

  • Hou X-G, Bergström J (1997) Arthropods of the Lower Cambrian Chengjiang fauna, southwest China. Fossils Strata 45:1–116

    Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Hughes CL, Kaufman TC (2002) Exploring myriapod segmentation: the expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev Biol 246:47–61

    Article  CAS  Google Scholar 

  • Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157

    Article  PubMed  CAS  Google Scholar 

  • 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 110:245–248

    Article  PubMed  CAS  Google Scholar 

  • 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 411:506–508

    Article  CAS  Google Scholar 

  • 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 1–72

    Google Scholar 

  • 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 268:89–104

    Article  PubMed  CAS  Google Scholar 

  • 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 355–385

    Google Scholar 

  • Jockusch EL, Ober KA (2004) Hypothesis testing in evolutionary developmental biology: a case study from insect wings. J Heredity 95:382–396

    Article  CAS  Google Scholar 

  • Kadner D, Stollewerk A (2004) Neurogenesis in the chilopod Lithobius forficatus suggests more similarities to chelicerates than to insects. Dev Genes Evol 214:367–379

    Article  PubMed  CAS  Google Scholar 

  • Kjellsvig-Waering EN (1986) A restudy of the fossil Scorpionida of the world. Palaeontogr Am 55:1–287

    Google Scholar 

  • Kuratani S (2003) Evolutionary developmental biology and vertebrate head segmentation: a perspective from developmental constraint. Theory Biosci 122:230–251

    Article  Google Scholar 

  • 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 270:2860–2868

    Article  PubMed  CAS  Google Scholar 

  • Lauterbach K-E (1973) Schlüsselereignisse in der Evolution der Stammgruppe der Euarthropoda. Zool Beitr (NF) 19:251–299

    Google Scholar 

  • Lauterbach K-E (1980a) Schlüsselereignisse in der Evolution des Grundplans der Mandibulata (Arthropoda). Abh Naturwiss Ver Hamburg NF 23:105–161

    Google Scholar 

  • Lauterbach K-E (1980b) Schlüsselereignisse in der Evolution des Grundplans der Arachnata (Arthropoda). Abh Naturwiss Ver Hamburg NF 23:163–327

    Google Scholar 

  • 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 206:35–45

    Article  CAS  Google Scholar 

  • Maas A, Waloszek D (2001) Cambrian derivatives of the early arthropod stem lineage, pentastomids, tardigrades and lobopodians—an ‘Orsten’ perspective. Zool Anz 240:451–459

    Google Scholar 

  • 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 14:158–166

    Article  Google Scholar 

  • 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 31:178–191

    Article  PubMed  CAS  Google Scholar 

  • Manton SM (1928) On the embryology of the crustacean Nebalia bipes. Phil Trans R Soc Lond B 223:163–238

    Google Scholar 

  • 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 233:483–580

    Google Scholar 

  • 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 205:424–431

    Article  Google Scholar 

  • Maxmen A, Browne WE, Martindale MQ, Giribet G (2005) Neuroanatomy of sea spiders implies an appendicular origin of the protocerebral segment. Nature 437:1144–1148

    Article  PubMed  CAS  Google Scholar 

  • 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 34:471–480

    Article  Google Scholar 

  • Meisenheimer J (1902) Beiträge zur Entwicklungsgeschichte der Pantopoden. I. Die Entwicklung von Ammothea echinata Hodge bis zur Ausbildung derLarvenform. Zeitschr Wiss Zool 72:191–248

    Google Scholar 

  • Minelli A (2003) The origin and evolution of appendages. Int J Dev Biol 47:573–581

    PubMed  Google Scholar 

  • Minelli A, Fusco G (2004) Evo–devo perspectives on segmentation: model organisms, and beyond. Trends Ecol Evol 19:423–429

    Article  PubMed  Google Scholar 

  • 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 211:232–243

    Article  PubMed  CAS  Google Scholar 

  • 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 213:9–17

    PubMed  Google Scholar 

  • Müller KJ, Walossek D (1986) Martinssonia elongata gen. et sp.n., a crustacean-like euarthropod from the Upper Cambrian ‘Orsten’ of Sweden. Zool Scr 15:73–92

    Article  Google Scholar 

  • 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 212:330–337

    Article  PubMed  CAS  Google Scholar 

  • 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 21:770–780

    Article  CAS  Google Scholar 

  • Nielsen C (2001) Animal evolution. Interrelationships of the living phyla, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Nielsen C (2005a) Trochophora larvae and adult body regions in annelids: some conclusions. Hydrobiologia 535/536:23–24

    Article  Google Scholar 

  • Nielsen C (2005b) Larval and adult brains. Evol Dev 7:483–489

    Article  PubMed  Google Scholar 

  • 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 14:115–125

    Article  Google Scholar 

  • Northcutt RG (2005) The new head hypothesis revisited. J Exp Zool (Mol Dev Evol) 304B:274–297

    Article  Google Scholar 

  • Nulsen C, Nagy LM (1999) The role of wingless in the development of multibranched crustacean limbs. Dev Genes Evol 209:340–348

    Article  PubMed  CAS  Google Scholar 

  • Oishi S (1959) Studies on the teloblasts in the decapod embryo I. Origin of teloblasts in Heptacarpus rectirostris (Stimpson). Embryol 4:283–309

    Article  Google Scholar 

  • 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 217–269

    Google Scholar 

  • 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 45:869–876

    PubMed  CAS  Google Scholar 

  • Olsson L, Ericsson, R, Cerny R (2005) Vertebrate head development: segmentation, novelties, and homology. Theory Biosci 124:145–163

    Article  PubMed  Google Scholar 

  • Osborne PW, Dearden PK (2005) Expression of Pax group III genes in the honey bee (Apis mellifera). Dev Genes Evol 215:499–508

    Article  PubMed  CAS  Google Scholar 

  • Page DT (2004) A mode of arthropod brain evolution suggested by Drosophila commissure development. Evol Dev 6:25–31

    Article  PubMed  Google Scholar 

  • Panganiban G, Sebring A, Nagy L, Carroll S (1995) The development of crustacean limbs and the evolution of arthropods. Science 270:1363–1366

    PubMed  CAS  Google Scholar 

  • Patel NH, Kornberg TB, Goodman CS (1989) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212

    PubMed  CAS  Google Scholar 

  • 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 411–419

    Google Scholar 

  • 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 208:547–557

    Article  PubMed  CAS  Google Scholar 

  • Pflugfelder O (1948) Entwicklung von Paraperipatus anboinensis n. sp. Zool Jb Anat 69:443–492

    Google Scholar 

  • 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 2:1–10

    Article  PubMed  Google Scholar 

  • 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 208:142–150

    Article  PubMed  CAS  Google Scholar 

  • Pross A (1966) Untersuchungen zur Entwicklungsgeschichte der Araneae (Pardosa hortensis (Thorell)) unter besonderer Berücksichtigung des vorderen Prosomaabschnitts. Z Morph Ökol Tiere 58:38–108

    Article  Google Scholar 

  • 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 260:97–112

    Article  PubMed  CAS  Google Scholar 

  • 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 211:467–477

    Article  PubMed  CAS  Google Scholar 

  • 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 265:119–140

    Article  CAS  Google Scholar 

  • 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 13:1876–1881

    Article  PubMed  CAS  Google Scholar 

  • Pultz MA, Pitt JN, Alto NM (1999) Extensive zygotic control of the anteroposterior axis in the wasp Nasonia vitripennis. Development 126:701–710

    PubMed  CAS  Google Scholar 

  • 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 132:3705–3715

    Article  PubMed  CAS  Google Scholar 

  • Ramsköld L, Edgecombe GD (1991) Trilobite monophyly revisited. Hist Biol 4:267–283

    Article  Google Scholar 

  • Rempel JG (1975) The evolution of the insect head: the endless dispute. Quaest Ent 11:7–25

    Google Scholar 

  • Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136

    Article  Google Scholar 

  • Richter S, Wirkner C (2004) Kontroversen in der phylogenetischen Systematik der Euarthropoda. Sber Ges Naturf Freunde Berlin (NF) 43:73–102

    Google Scholar 

  • Rogers BT, Kaufman TC (1997) Structure of the insect head in ontogeny and phylogeny: a view from Drosophila. Int Rev Cytol 174:1–84

    Article  PubMed  CAS  Google Scholar 

  • 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 4:96–110

    Article  PubMed  CAS  Google Scholar 

  • Rohrschneider I (1968) Beiträge zur Entwicklung des Vorderkopfes und der Mundregion von Periplaneta americana. Zool Jb Anat 85:537–578

    Google Scholar 

  • 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 206:237–246

    Article  CAS  Google Scholar 

  • 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 116:111–125

    PubMed  CAS  Google Scholar 

  • 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 203:298–303

    Article  Google Scholar 

  • 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 91:8363–8367

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Rhaesa A, Bartolomaeus T, Lemburg C, Ehlers U, Garey JR (1998) The position of the Arthropoda in the phylogenetic system. J Morphol 238:263–285

    Article  Google Scholar 

  • Schneuwly S, Klemenz R, Gehring WJ (1987) Redesigning the body plan of Drosophila by ectopic expression of the homeotic gene Antennapedia. Nature 325:816–818

    Article  PubMed  CAS  Google Scholar 

  • Scholl G (1963) Embryologische Untersuchungen an Tanaidaceen (Heterotanais oerstedi Kröyer). Zool Jb Anat 80:500–554

    Google Scholar 

  • Scholl G (1969) Die Embryonalentwicklung des Kopfes und Prothorax von Carausius morosus Br. (Insecta, Phasmida). Z Morph Tiere 65:1–142

    Article  Google Scholar 

  • Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154

    Article  Google Scholar 

  • Scholtz G (1995) Head segmentation in Crustacea—an immunocytochemical study. Zoology 98:104–114

    Google Scholar 

  • 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 317–332

    Google Scholar 

  • Scholtz G (2001) Evolution of developmental patterns in arthropods-the contribution of gene expression to morphology and phylogenetics. Zoology 103:99–111

    CAS  Google Scholar 

  • Scholtz G (2002) The Articulata hypothesis—or what is a segment? Organ Divers Evol 2:197–215

    Article  Google Scholar 

  • 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 489–501

  • 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 3–16

    Google Scholar 

  • Scholtz G (2005) Homology and ontogeny: pattern and process in comparative developmental biology. Theory Biosci 124:121–143

    Article  PubMed  Google Scholar 

  • 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 139–165

    Google Scholar 

  • 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 38:471–478

    PubMed  CAS  Google Scholar 

  • 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 42:801–810

    PubMed  CAS  Google Scholar 

  • 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 211:76–82

    Article  PubMed  CAS  Google Scholar 

  • Schröder R (2003) The genes orthodenticle and hunchback substitute for bicoid in the beetle Tribolium. Nature 422:621–625

    Article  PubMed  CAS  Google Scholar 

  • Seaver EC (2003) Segmentation: mono or polyphyletic? Int J Dev Biol 47:583–595

    PubMed  Google Scholar 

  • 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 289:179–194

    Article  PubMed  CAS  Google Scholar 

  • 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 7:312–326

    Article  PubMed  Google Scholar 

  • Selden PA (1981) Functional morphology of the prosoma of Baltoeurypterus tetragonophthalmus (Fischer) (Chelicerata: Eurypterida). Trans R Soc Edinburgh: Earth Sci 72:9–48

    Google Scholar 

  • Semmler H (2005) Immuncytochemische Studien zur larvalen Myo- und Neuroanatomie von Balanus improvisus (Crustacea, Cirripedia, Thecostraca). Diplom Thesis: Humboldt-Universität zu Berlin

  • Shiga Y, Yasumoto R, Yamagata H, Hayashi S (2002) Evolving role of Antennapedia protein in arthropod limb patterning. Development 129:3555–3561

    PubMed  CAS  Google Scholar 

  • Siewing R (1963) Das Problem der Arthropodenkopfsegmentierung. Zool Anz 170:429–468

    Google Scholar 

  • Siewing R (1969) Lehrbuch der vergleichenden Entwicklungsgeschichte der Tiere. Parey, Hamburg

    Google Scholar 

  • Simonnet F, Deutsch J, Quéinnec E (2004) hedgehog is a segment polarity gene in a crustacean and a chelicerate. Dev Genes Evol 214:527–545

    Article  CAS  Google Scholar 

  • Snodgrass RE (1960) Facts and theories concerning the insect head. Smithson Misc Collect 142:1–61

    Google Scholar 

  • Starck D (1963) Die Metamerie des Kopfes der Wirbeltiere. Zool Anz 170:393–428

    Google Scholar 

  • 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 55–71

    Google Scholar 

  • Størmer L (1944) On the relationships and phylogeny of fossil and recent Arachnomorpha. Skrift Utgitt Norske Vidensk-akad Oslo I Math-Naturvitensk Klasse 5:1–158

    Google Scholar 

  • 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 13:331–336

    Article  Google Scholar 

  • Tautz D (2004) Segmentation. Dev Cell 7:301–312

    Article  PubMed  CAS  Google Scholar 

  • Telford MJ, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci U S A 95:10671–10675

    Article  PubMed  CAS  Google Scholar 

  • Thomas RH, Telford MJ (1999) Appendage development in embryos of the oribatid mite Archegozetes longisetus (Acari, Oribatei, Thrypochthoniidae) Acta Zool 80:193–200

    Article  Google Scholar 

  • Tiegs OW (1940) The embryology and affinities of the Symphyla, based on a study of Hanseniella agilis. Q J Microsc Sci 82:1–225

    Google Scholar 

  • Tomsa JM, Langeland JA (1999) Otx expression during lamprey embryogenesis provides insights into the evolution of the vertebrate head and jaw. Dev Biol 207:26–37

    Article  PubMed  CAS  Google Scholar 

  • 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 747:245–276

    Google Scholar 

  • 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 209:31–39

    Article  PubMed  CAS  Google Scholar 

  • Ungerer P, Wolff C (2005) External morphology of limb development in the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89–99

    Article  Google Scholar 

  • 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 32:103–123

    Article  Google Scholar 

  • Urbach R, Technau G (2003b) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130:3621–3637

    Article  PubMed  CAS  Google Scholar 

  • Urbach R, Technau G, Breidbach O (2003) Spatial and temporal pattern of neuroblasts, proliferation, and engrailed expression during early brain development. Arthrop Struct Dev 32:125–140

    Article  Google Scholar 

  • 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 32:349–383

    Article  Google Scholar 

  • von Wistinghausen C (1891) Untersuchungen über die Entwicklung von Nereis dumerilii. Mitt Zool Stat Neapel 10:41–74

    Google Scholar 

  • 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 83:235–326

    Google Scholar 

  • 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 39:165–176

    Article  Google Scholar 

  • Walossek D (1993) The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32:3–202

    Google Scholar 

  • 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 2000:69–87

  • 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 45:421–446

    Article  Google Scholar 

  • 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 23:409–427

    Google Scholar 

  • Waloszek D, Chen J, Maas A, Wang X (2005) Early Cambrian arthropods—new insights into arthropod head and structural evolution. Arthrop Struct Dev 34:189–205

    Article  Google Scholar 

  • Weber H (1952) Morphologie, Histologie und Entwicklungsgeschichte der Articulaten II. Die Kopfsegmentierung und die Morphologie des Kopfes überhaupt. Fortschr Zool 9:18–231

    Google Scholar 

  • Weygoldt P (1985) Ontogeny of the arachnid central nervous system. In: Barth FG (ed) Neurobiology of arachnids. Springer, Berlin Heidelberg New York, pp 20–37

    Google Scholar 

  • Whittington HB (1975) Trilobites with appendages from the Middle Cambrian Burgess Shale, British Columbia. Fossils Strata 4:97–136

    Google Scholar 

  • Whittington HB (1980) Exoskeleton, moult stage, appendage morphology and habits of the Middle Cambrian trilobite Olenoides serratus. Palaeontology 23:171–204

    Google Scholar 

  • Winter G (1980) Beiträge zur Morphologie und Embryologie des vorderen Körperabschnitts (Cephalosoma) der Pantopoda Gerstaecker, 1863. Z Zoolog Syst Evol Forsch 18:27–61

    Google Scholar 

  • Wolff C (2004) Die Beinentwicklung des amphipoden Krebses Orchestia cavimana (Peracarida, Malacostraca - eine zellgenealogische Studie. Doctoral Thesis, Humboldt-Universität zu Berlin

  • Woltereck R (1905) Zur Kopffrage der Anneliden. Verh Dtsch Zool Ges 15:154–186

    Google Scholar 

  • 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 214:128–133

    Article  PubMed  CAS  Google Scholar 

  • 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 182:270–283

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Jean Deutsch and Michel Veuille, the organizers of the meeting “Development and Phylogeny of Arthropods,” Paris 2005, for the invitation to GS to present our thoughts on head evolution. Nikola-Michael Prpic made helpful comments on an earlier version of the manuscript. We are grateful to Henrike Semmler for her pictures of the innervation of the frontal filaments in nauplius larvae of cirripedes and Carsten Wolff for the picture of the embryonic head of Orchestia cavimana (Fig. 4). Alfred Palissa helped with literature about Protura. This article benefited tremendously from the inspiring discussions with the students in the seminar “Phylogeny of Recent and Fossil Taxa” held at the Humboldt-University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerhard Scholtz.

Additional information

Communicated by guest editors Jean Deutsch and Gerhard Scholtz

Electronic supplementary material

Below is the link to the supplementary material.

427_2006_85_MOESM1_ESM.doc

427_2006_85_MOESM2_ESM.htm

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scholtz, G., Edgecombe, G.D. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence . Dev Genes Evol 216, 395–415 (2006). https://doi.org/10.1007/s00427-006-0085-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00427-006-0085-4

Keywords

Navigation