Zoomorphology

, Volume 128, Issue 3, pp 263–274 | Cite as

Cleavage and gastrulation in Pycnogonum litorale (Arthropoda, Pycnogonida): morphological support for the Ecdysozoa?

Original Paper

Abstract

The early cleavage and gastrulation of the pycnogonid Pycnogonum litorale is investigated in detail by fluorescence microscopy, confocal laser scanning microscopy, and histology. The cleavage is holoblastic with equally sized blastomeres and an irregular radial pattern. There is no stereotypic cell lineage, and timing and spindle directions of individual mitoses vary to a high degree. Gastrulation begins at the 63-cell stage with the retardation and enlargement of a cell which adopts the form of a bottle and fills the interior of the egg, followed by immigration and epiboly of smaller cells surrounding the large bottle-shaped cell. The gastrulation site marks the dorsal side of the embryo and the stomodaeum forms adjacent to the area of gastrulation. The pattern of the early development of Pycnogonum is compared with that of other Pycnogonida resulting in a putative ground pattern of pycnogonid development. Furthermore, our results are discussed in the wider framework of putative arthropod and cycloneuralian relationships. This comparison implies morphological support for the Ecdysozoa.

Keywords

Cell lineage Articulata Spiral cleavage Germ layers Evolution 

References

  1. 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. doi:10.1038/387489a0 PubMedCrossRefGoogle Scholar
  2. Alwes F, Scholtz G (2004) Cleavage and gastrulation of the euphausiacean Meganyctiphanes norvegica (Crustacea, Malacostraca). Zoomorphology 123:125–137. doi:10.1007/s00435-004-0095-6 CrossRefGoogle Scholar
  3. Anderson DT (1969) On the embryology of the cirripede crustacean Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of crustacean phylogenetic relationships. Philos Trans R Soc Lond 256:183–235. doi:10.1098/rstb.1969.0041 CrossRefGoogle Scholar
  4. Anderson DT (1973) Embryology and phylogeny in annelids and arthropods. Pergamon Press, OxfordGoogle Scholar
  5. Arango CP, Wheeler WC (2007) Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23:1–39. doi:10.1111/j.1096-0031.2007.00143.x CrossRefGoogle Scholar
  6. Bamber RN (2007) A holistic re-interpretation of the phylogeny of the Pycnogonida Latreille, 1810 (Arthropoda). Zootaxa 1668:295–312Google Scholar
  7. Bamber RN, El Nagar A (2009) Pycnobase: World Pycnogonid Database. Available online at http://www.marinespecies.org/pycnobase/. Accessed 20 February 2009
  8. Behrens W (1984) Larvenentwicklung und Metamorphose von Pycnogonum litorale (Chelicerata, Pantopoda). Zoomorphology 104:266–279. doi:10.1007/BF00312008 CrossRefGoogle Scholar
  9. Brenneis G, Ungerer P, Scholtz G (2008) The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment. Evol Dev 10:717–724PubMedGoogle Scholar
  10. Claypole AM (1898) The embryology and oogenesis of Anurida maritima. J Morphol 14:219–300. doi:10.1002/jmor.1050140205 CrossRefGoogle Scholar
  11. Dearden PK, Donly C, Grbic M (2002) Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129:5461–5472. doi:10.1242/dev.00099 PubMedCrossRefGoogle Scholar
  12. Dogiel V (1913) Embryologische Studien an Pantopoden. Z Wiss Zool 107:575–741Google Scholar
  13. Dohle W (1964) Die Embryonalentwicklung von Glomeris marginata (Villers) im Vergleich zur Entwicklung anderer Diplopoden. Zool Jb Anat 81:241–310Google Scholar
  14. Dohle W (1996) Spiralia. In: Westheide W, Rieger R (eds) Spezielle Zoologie, Teil 1: Einzeller und Wirbellose Tiere. Gustav Fischer Verlag, Stuttgart, pp 205–209Google Scholar
  15. Dohrn A (1881) Die Pantopoden des Golfes von Neapel und der angrenzenden Meeres-Abschnitte. Fauna & Flora des Golfes von Neapel und der angrenzenden Meeres-Abschnitte 3:1–252Google Scholar
  16. Dunlop JA, Arango CP (2005) Pycnogonid affinities: a review. J Zool Syst Evol Res 43:8–21. doi:10.1111/j.1439-0469.2004.00284.x CrossRefGoogle Scholar
  17. Dunn CW et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. doi:10.1038/nature06614 PubMedCrossRefGoogle Scholar
  18. Fuchs K (1914) Die Keimbahnentwicklung von Cyclops viridis Jurine. Zool Jb Anat 38:103–156Google Scholar
  19. Gabriel WN, McNuff R, Patel SK, Gregory TR, Jeck WR, Jones CD, Goldstein B (2007) The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev Biol 312:545–559. doi:10.1016/j.ydbio.2007.09.055 PubMedCrossRefGoogle Scholar
  20. Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801. doi:10.1242/dev.00155 PubMedCrossRefGoogle Scholar
  21. Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161. doi:10.1038/35093097 PubMedCrossRefGoogle Scholar
  22. Hejnol A, Schnabel R (2005) The eutardigrade Thulinia stephaniae has an indeterminate development and the potential to regulate early blastomere ablations. Development 132:1349–1361. doi:10.1242/dev.01701 PubMedCrossRefGoogle Scholar
  23. Hejnol A, Schnabel R (2006) What a couple of dimensions can do for you: comparative developmental studies using 4D microscopy—examples from tardigrade development. Integr Comp Biol 46:151–161. doi:10.1093/icb/icj012 CrossRefGoogle Scholar
  24. Hertzler PL (2005) Cleavage and gastrulation in the shrimp Penaeus (Litopenaeus) vannamei (Malacostraca, Decapoda, Dendrobranchiata). Arthropod Struct Dev 34:455–469Google Scholar
  25. Hertzler PL, Clark WHJ (1992) Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116:127–140PubMedGoogle Scholar
  26. Heuer CM, Loesel R (2008) Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida). Cell Tissue Res 331:713–714. doi:10.1007/s00441-007-0535-y PubMedCrossRefGoogle Scholar
  27. Hoek PPC (1881) Report on the Pycnogonida, dredged by HMS Challenger during the years 1873–76. Zool Chall Exp 10:1–167Google Scholar
  28. 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 Press, Boca Raton, pp 355–385Google Scholar
  29. Jura C (1966) Origin of the endoderm and embryogeneis of the alimentary system in Tetradontophora bielanensis (Waga) (Collembola). Acta Biol Cracow Zool 9:95–102Google Scholar
  30. Kozloff EN (2007) Stages of development, from first cleavage to hatching, of an Echinoderes (Phylum Kinorhyncha: Class Cyclorhagida). Cah Biol Mar 48:199–206Google Scholar
  31. Kühn A (1913) Die Sonderung der Keimesbezirke in der Entwicklung der Sommereier von Polyphemus pediculus de Geer. Zool Jb Anat 35:243–340Google Scholar
  32. Lang K (1953) Die Entwicklung des Eies von Priapulus caudatus Lam. und die systematische Stellung der Priapuliden. Ark Zool 5:321–348Google Scholar
  33. Longhorn SJ, Foster PG, Vogler AP (2007) The nematode-arthropod clade revsited: phylogenomic analyses from ribosomal protein genes misled by shared evolutionary biases. Cladistics 23:130–144. doi:10.1111/j.1096-0031.2006.00132.x CrossRefGoogle Scholar
  34. Malakhov VV, Spiridonov SE (1984) The embryogenesis of Gordius sp. from Turkmenia, with special reference to the position of the Nematomorpha in the animal kingdom. Zool Zh 63:1285–1297 Russian with English summaryGoogle Scholar
  35. Mallatt J, Giribet G (2006) Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phyl Evol 40:772–794. doi:10.1016/j.ympev.2006.04.021 CrossRefGoogle Scholar
  36. Meisenheimer J (1902) Beiträge zur Entwicklungsgeschichte der Pantopoden. I. Die Entwicklung von Ammothea echinata Hodge bis zur Ausbildung der Larvenform. Z Wiss Zool 72:191–248Google Scholar
  37. Montgomery T (1904) Development and structure of the larva of Paragordius. Proc Acad Nat Sci Phila 56:738–755Google Scholar
  38. Morgan TH (1891) A contribution to the embryology and phylogeny of the pycnogonids. Stud Biol Lab Johns Hopkins Univ 5:1–76Google Scholar
  39. Moritz KB, Sauer HW (1996) Boveri’s contributions to developmental biology–a challenge for today. Int J Dev Biol 40:27–47PubMedGoogle Scholar
  40. Mühldorf A (1914) Beiträge zur Entwicklungsgeschichte der Gordius Larve. Z Wiss Zool 111:1–75Google Scholar
  41. Nachtwey R (1925) Untersuchungen über die Keimbahn, Organogenese und Anatomie von Asplanchna priodonta Gosse. Z Wiss Zool 126:239–492Google Scholar
  42. Nakamura K, Kano Y, Suzuki N, Namatame T, Kosaku A (2007) 18S rRNA phylogeny of sea spiders with emphasis on the position of Rhynchothoracidae. Mar Biol 153:213–223CrossRefGoogle Scholar
  43. Nielsen C (2001) Animal evolution, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  44. Pilato G, Binda MG, Biondi O, D’Urso V, Lisi O, Marletta A, Maugeri S, Nobile V, Rappazzo G, Sabella G, Sammartano F, Turrisi G, Viglianisi F (2005) The clade Ecdysozoa, perplexities and questions. Zool Anz 244:43–50. doi:10.1016/j.jcz.2005.04.001 CrossRefGoogle Scholar
  45. Podsiadlowski L, Braband A (2006) The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida). BMC Genomics 7:284. doi:10.1186/1471-2164-7-284 PubMedCrossRefGoogle Scholar
  46. Richter S, Wirkner C (2004) Kontroversen in der phylogenetischen Systematik der Euarthropoda. Sber Ges Naturf Freunde Berl NF 43:73–102Google Scholar
  47. Roeding F, Hagner-Holler S, Ruhberg H, Ebersberger I, von Haeseler A, Kube M, Reinhardt R, Burmester T (2007) EST sequencing of Onychophora and phylogenomic analysis of Metazoa. Mol Phylogenet Evol 45:942–951PubMedGoogle Scholar
  48. Sanchez S (1959) Le développement des Pycnogonides et leurs affinités avec les Arachnides. Arch Zool Exp Gen 98:1–102Google Scholar
  49. Schierenberg E (2005) Unusual cleavage and gastrulation in a freshwater nematode: developmental and phylogenetic implications. Dev Genes Evol 215:103–108. doi:10.1007/s00427-004-0454-9 PubMedCrossRefGoogle Scholar
  50. Schierenberg E, Schulze J (2008) Many roads lead to Rome: different ways to construct a nematode. In: Minelli A, Fusco G (eds) Evolving pathways: key themes in evolutionary developmental biology. Cambridge University Press, Cambridge, pp 261–280Google Scholar
  51. 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. doi:10.1002/(SICI)1097-4687(199812)238:3<263::AID-JMOR1>3.0.CO;2-L CrossRefGoogle Scholar
  52. 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 & Hall, London, pp 317–332Google Scholar
  53. Scholtz G (2002) The Articulata hypothesis—or what is a segment? Org Divers Evol 2:197–215. doi:10.1078/1439-6092-00046 CrossRefGoogle Scholar
  54. 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
  55. Scholtz G, Edgecombe GD (2006) The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Dev Genes Evol 216:395–415. doi:10.1007/s00427-006-0085-4 PubMedCrossRefGoogle Scholar
  56. Scholtz G, Wolff C (2002) Cleavage, gastrulation, and germ disc formation of the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Contrib Zool 71:9–28Google Scholar
  57. Sekiguchi K, Nakamura K, Onuma S (1971) Egg-carrying habit and embryonic development in a pycnogonid, Propallene longiceps. Zool Mag 80:137–139 Japanese with English summaryGoogle Scholar
  58. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119. doi:10.1016/0012-1606(83)90201-4 PubMedCrossRefGoogle Scholar
  59. Teuchert G (1968) Zur Fortpflanzung und Entwicklung der Macrodasyoidea (Gastrotricha). Z Morphol Tiere 63:343–418. doi:10.1007/BF00391930 CrossRefGoogle Scholar
  60. 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
  61. Tiegs OW (1947) The development and affinities of the Pauropoda based on a study of Pauropus silvaticus. Q J Microsc Sci 88(165–267):275–336Google Scholar
  62. Tomaschko K-H, Wilhelm E, Bückmann D (1997) Growth and reproduction of Pycnogonum litorale (Pycnogonida) under laboratory conditions. Mar Biol (Berl) 129:595–600. doi:10.1007/s002270050201 CrossRefGoogle Scholar
  63. 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. Arthropod Struct Dev 32:349–383. doi:10.1016/j.asd.2003.09.004 PubMedCrossRefGoogle Scholar
  64. 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. doi:10.1046/j.1439-0469.2001.00177.x CrossRefGoogle Scholar
  65. Wennberg SA, Janssen R, Budd GE (2008) Early embryonic development of the priapulid worm Priapulus caudatus. Evol Dev 10:326–338PubMedGoogle Scholar
  66. Weygoldt P (1960) Embryologische Untersuchungen an Ostrakoden: die Entwicklung von Cyprideis litoralis (G.S. Brady) (Ostracoda, Podocopa, Cytheridae). Zool Jb Anat 78:369–426Google Scholar
  67. Weygoldt P (1979) Gastrulation in the Arthropoda? Fortschr Zool Syst Evolutionsforsch 1:73–81Google Scholar
  68. Wolff C, Scholtz G (2002) Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev Biol 250:44–58. doi:10.1006/dbio.2002.0789 PubMedCrossRefGoogle Scholar
  69. Zrzavý J, Hypša V, Vlášková M (1997) Arthropod phylogeny: taxonomic congruence, total evidence and conditional combination approaches to morphological and molecular data sets. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 97–107Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Institut für Biologie/Vergleichende ZoologieHumboldt-Universität zu BerlinBerlinGermany
  2. 2.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK

Personalised recommendations