Advertisement

Development Genes and Evolution

, Volume 229, Issue 4, pp 103–124 | Cite as

The cleavage pattern of calanoid copepods—a case study

  • Günther LooseEmail author
  • Gerhard ScholtzEmail author
Original Article

Abstract

Many crustacean groups show stereotyped cleavage patterns during early ontogeny. However, these patterns differ between the various major crustacean taxa, and a general mode is difficult to extract. Previous studies suggested that also copepods undergo an early cleavage with a more or less stereotyped pattern of blastomere divisions and fates. Yet, copepod embryology has been largely neglected. The last investigation of this kind dates back more than a century and the results are somewhat contradictory when compared with those of other researchers. To overcome these problems, we studied the early development of a so far undescribed calanoid copepod species, Skistodiaptomus sp., applying histochemical staining, confocal laser scanning microscopy, and bifocal 4D microscopy. The blastomere arrangement of the four-cell stage of this species varies to a large degree. It can either form a typical radial pattern with the four blastomeres lying in one plane or a tilted orientation of the axes connecting the sister cells of the previous division. In both cases, a stereotyped division pattern is maintained inside each quadrant during subsequent cleavages. In addition, we found two types of blastomere arrangements with a mirror symmetry. Most divisions within the quadrants follow the perpendicularity rule until the eighth cleavage. Deviations from this rule occur only in the narrow regions where the different quadrants touch and near the site of gastrulation. Gastrulation is initiated around the descendants of one individually identifiable blastomere of the 16-cell stage. This cell divides in a specific manner forming a characteristic cell arrangement, the gastrulation triangle. This gastrulation triangle initiates the internalization process of the gastrulation and it is encircled by another characteristic cell type, the crown cells. Our observations reveal several similarities to the early development of Calanus finmarchicus, another calanoid species. These relate to blastomere arrangements and divisions and the pattern of gastrulation. As Calanoida represent a basal or near basal branch of the copepod tree, this description will provide the ground for reconstruction of the cleavage pattern of the last common ancestor of Copepoda.

Keywords

Copepoda Calanoida Cleavage Gastrulation Cell lineage Radial cleavage 

Notes

Acknowledgments

We are thankful to Carsten Lüter for granting access to the confocal microscope system in his lab, to Thomas Stach for supplying the equipment for bifocal 4D-Microscopy, to Christopher Grossmann for support with manual blastomere segmentation, and to Khashayar Rhazgandi for providing microalgae and assisting with their culture. This research was funded in the framework of the Cluster of Excellence: “Image Knowledge Gestaltung,” project “Dynamic Form” at the Humboldt-Universität zu Berlin.

Supplementary material

427_2019_634_MOESM1_ESM.pdf (37.6 mb)
Supplemental file 1 Cell lineage ofSkistodiaptomus sp. Lineage tree of L-type cleavage pattern, reconstructed from 4D-recordings. The timing of division events is based on estimates. Labels of individual cells are given left of the branches until the sixth cleavage round. The branches are color coded according to quadrant identity (A, B, C or D- quadrant), crown cells or gastrulation triangle. The depicted time period represents approximately 35 h of development. (PDF 37.5 mb)
427_2019_634_MOESM2_ESM.pdf (37.6 mb)
Supplemental file 2 Pattern of cleavage seven. Schematic depictions of blastomere arrangement and cell genealogy 123 cell embryo. The quadrants of the embryo are mapped around the pole of hemisphere II, which lies in the middle of each drawing. Quadrant identities are color coded, cell names are labeled. Cells of the gastrulation have not divided since 63 cell stage. A. L-type cleavage. B. R-type cleavage. (PDF 37.5 mb)

References

  1. Alwes F, Scholtz G (2004) Cleavage and gastrulation of the euphausiacean Meganyctiphanes norvegica (Crustacea, Malacostraca). Zoomorphology 123:125–137CrossRefGoogle Scholar
  2. Alwes F, Scholtz G (2014) The early development of the onychopod cladoceran Bythotrephes longimanus (Crustacea, Branchiopoda). Front Zool 11:10CrossRefGoogle Scholar
  3. Amma K (1911) Über die Differenzierung der Keimbahnzellen bei den Copepoden. Arch Zellforsch 6:497–576Google Scholar
  4. Benedetti I, Mola L, Monari E, Sabatini MA, Marini M, Fratello B (1989) Preliminary findings on the development of the parasitic copepod Lernaea cyprinacea L. from cleavage to hatching. Ital J Zool 56:7–11Google Scholar
  5. Biffis C, Alwes F, Scholtz G (2009) Cleavage and gastrulation of the dendrobranchiate shrimp Penaeus monodon (Crustacea, Malacostraca, Decapoda). Arthr Struct Dev 38:527–540CrossRefGoogle Scholar
  6. Blaxter JH, Douglas B, Tyler PA, Mauchline J (1998) The biology of calanoid copepods, vol 33. Academic PressGoogle Scholar
  7. Bradford-Grieve JM (2002) Calanoida: families. Version 1: 2. http://crustacea.net/crustace/calanoida/index.htm. Accessed 10 June 2017
  8. Dallwitz MJ, Paine TA, Zurcher EJ (2000) Principles of interactive keys. Web-based document http://biodiversity. uno. edu/delta, 3. Accessed 10 June 2017Google Scholar
  9. Eyun SI (2017) Phylogenomic analysis of Copepoda (Arthropoda, Crustacea) reveals unexpected similarities with earlier proposed morphological phylogenies. BMC Evol Biol 17:23CrossRefGoogle Scholar
  10. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299Google Scholar
  11. Fuchs K (1914) Die Keimbahnentwicklung von Cyclops viridis Jurine. Zool Jb Anat 38:103–146Google Scholar
  12. Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801CrossRefGoogle Scholar
  13. Gorham FP (1895) The cleavage of the egg of Virbius zostericola, Smith. A contribution to Crustacean cytogeny. J Morphol 11:741–746CrossRefGoogle Scholar
  14. Grobben C (1881) Die Entwicklungsgeschichte von Cetochilus septentrionalis Goodsir Arb Zool Inst Univ Wien 3:1–40Google Scholar
  15. Gupta T, Extavour CG (2013) Identification of a putative germ plasm in the amphipod Parhyale hawaiensis. Evo Devo 4:34Google Scholar
  16. Häcker V (1897) Die Keimbahn von Cyclops. Neue Beiträge zur Kenntniss der Geschlechtszellen-Sonderung. Arch Mikrosk Anat 49:35–91Google Scholar
  17. Hertzler PL, Clark WH (1992) Cleavage and gastrulation in the shrimp Sicyonia ingentis: invagination is accompanied by oriented cell division. Development 116:127–140Google Scholar
  18. Ho J (1990) Phylogenetic analysis of copepod orders. J Crustac Biol 10:528–536CrossRefGoogle Scholar
  19. Humes AG (1994) How many copepods? In: Ferrari FD, Bradley BP (eds) Ecology and morphology of copepods. Hydrobiologia 292(293):1–7CrossRefGoogle Scholar
  20. Hunter JD (2007) Matplotlib: a 2D graphics environment. Comput Sci Eng 9:90–95CrossRefGoogle Scholar
  21. Huys R, Boxshall G (1991) Copepod evolution. The Ray Society, LondonGoogle Scholar
  22. Keller MD, Selvin RC, Claus W, Guillard RR (1987) Media for the culture of oceanic ultraphytoplankton 1, 2. J Phycol 23:633–638CrossRefGoogle Scholar
  23. Khodami S, McArthur JV, Blanco-Bercial L, Arbizu PM (2017) Molecular phylogeny and revision of copepod orders (Crustacea: Copepoda). Sci Rep UK 7:9164CrossRefGoogle Scholar
  24. Klann M, Scholtz G (2014) Early embryonic development of the freshwater shrimp Caridina multidentata (Crustacea, Decapoda, Atyidae). Zoomorphology 133:295–306CrossRefGoogle Scholar
  25. Kühn A (1913) Die Sonderung der Keimesbezirke in der Entwicklung der Sommereier von Polyphemus pediculus de Geer. Zool Jb Anat 35:243–340Google Scholar
  26. Kohler HJ (1976) Embryologische Untersuchungen an Copepoden: die Entwicklung von Lernaeocera branchialis L. 1767 (Crustacea, Copepoda, Lernaeoida, Lernaeidae). Zool Jb Anat 95:448–504Google Scholar
  27. McClendon JF (1907) On the development of parasitic copepods: part II. Biol Bull 12:53–88CrossRefGoogle Scholar
  28. Pawlak JB, Sellars MJ, Wood A, Hertzler PL (2010) Cleavage and gastrulation in the Kuruma shrimp Penaeus (Marsupenaeus) japonicus (Bate): a revised cell lineage and identification of a presumptive germ cell marker. Develop Growth Differ 52:677–692CrossRefGoogle Scholar
  29. Pedaschenko DD (1898) Die Embryonalentwickelung und Metamorphose von Lernaea branchialis L. Trav Soc Imp Nat St Petersbourg 26:247–306Google Scholar
  30. Pennerstorfer M, Scholtz G (2012) Early cleavage in Phoronis muelleri (Phoronida) displays spiral features. Evol Dev 14:484–500CrossRefGoogle Scholar
  31. Ponomarenko E (2014) The embryonic development of Elminius modestus Darwin, 1854 (Thecostraca: Cirripedia). Dissertation, Humboldt-Universität zu BerlinGoogle Scholar
  32. Sagawa K, Yamagata H, Shiga Y (2005) Exploring embryonic germ line development in the water flea, Daphnia magna, by zinc-finger-containing VASA as a marker. GEP 5:669–678Google Scholar
  33. Scheidegger G (1976) Stadien der Embryonalentwicklung von Eupagurus prideauxi Leach (Crustacea, Decapoda, Anomura) unter besonderer Berücksichtigung der Darmentwicklung und der am Dotterbau beteiligten Zelltypen. Zool Jb Anat 95:297–353Google Scholar
  34. Schminke HK (2007) Entomology for the copepodologist. J Plankton Res 29:i149–i162CrossRefGoogle Scholar
  35. Schimkewitsch W (1896) Studien über parasitische Copepoden. Z Wiss Zool 61:339–362Google Scholar
  36. Scholtz G, Wolff C (2002) Cleavage, gastrulation, and germ disc formation of the amphipod Orchestia cavimana (Crustacea, Malacostraca, Peracarida). Contrib Zool 71:9–28CrossRefGoogle Scholar
  37. Scholtz G, Wolff C (2013) Arthropod embryology: cleavage and germ band development. In: Minelli A, Fusco G, Boxshall G (eds) Arthropod biology and evolution—molecules, development, morphology. Springer, Heidelberg, pp 63–90CrossRefGoogle Scholar
  38. Scholtz G, Ponomarenko E, Wolff C (2009) Cirripede cleavage patterns and the origin of the Rhizocephala (Crustacea: Thecostraca). Arthrop Syst Phyl 67:219–228Google Scholar
  39. Stach T, Anselmi C (2015) High-precision morphology: bifocal 4D-microscopy enables the comparison of detailed cell lineages of two chordate species separated for more than 525 million years. BMC Biol 13:1–11CrossRefGoogle Scholar
  40. Strömberg JO (1971) Contribution to the embryology of bopyrid isopods with special reference to Bopyroides, Hemiarthrus, and Peseudione (Isopoda, Epicaridea). Sarsia 47:1–46CrossRefGoogle Scholar
  41. Van Beneden É, Bessels É (1868) Résumé d’un mémoire sur le mode de formation du blastoderme dans quelques groupes de crustacés. Bulletins de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique 25:434–448Google Scholar
  42. Witschi E (1934) On the determinative cleavage and yolk formation in the harpacticoid copepod Tisbe furcata (Baird). Biol Bull 67:335–340CrossRefGoogle Scholar
  43. Wolff C, Scholtz G (2002) Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev Biol 250:44–58CrossRefGoogle Scholar
  44. Wolff C et al. (2018) Multi-view light-sheet imaging and tracking with the MaMuT software reveals the cell lineage of a direct developing arthropod limb. eLife, 7Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Humboldt-Universität zu Berlin, Institut für BiologieVergleichende ZoologieBerlinGermany

Personalised recommendations