Advertisement

Development Genes and Evolution

, Volume 220, Issue 3–4, pp 89–105 | Cite as

Muscle development in the marbled crayfish—insights from an emerging model organism (Crustacea, Malacostraca, Decapoda)

  • Günther Jirikowski
  • Sabine Kreissl
  • Stefan Richter
  • Carsten Wolff
Original Article

Abstract

The development of the crustacean muscular system is still poorly understood. We present a structural analysis of muscle development in an emerging model organism, the marbled crayfish—a representative of the Cambaridae. The development and differentiation of muscle tissue and its relation to the mesoderm-forming cells are described using fluorescent and non-fluorescent imaging tools. We combined immunohistochemical staining for early isoforms of myosin heavy chain with phallotoxin staining of F-actin, which distinguishes early and more differentiated myocytes. We were thus able to identify single muscle precursor cells that serve as starting points for developing muscular units. Our investigations show a significant developmental advance in head appendage muscles and in the posterior end of the longitudinal trunk muscle strands compared to other forming muscle tissues. These findings are considered evolutionary relics of larval developmental features. Furthermore, we document the development of the muscular heart tissue from myogenic precursors and the formation and differentiation of visceral musculature.

Keywords

Marmorkrebs Development Muscle precursor Myogenesis Evolution 

Notes

Acknowledgements

The 4D9 anti-EN/INVECTED monoclonal antibody developed by Corey Goodman (University of California, Berkeley) was obtained from the Developmental Studies Hybridoma Bank, which was developed under the auspices of the NICHD and is maintained by The University of Iowa, Iowa City, IA 52242. We also express our gratitude to Frederike Alwes for instructions on crayfish care, egg handling, dissection, and staining. Thanks also to Lucy Cathrow for improving the English of the manuscript. This study was supported by the DFG grant Ri837/8-1 to SR, Wo1461/1-1 to CW.

References

  1. Abzhanov A, Kaufman TC (2000) Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 210:493–506CrossRefGoogle Scholar
  2. Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216:169–184CrossRefPubMedGoogle Scholar
  3. Baylies MK, Bate M, Gomez MR (1998) Myogenesis: a view from Drosophila. Cell 93:921–927CrossRefPubMedGoogle Scholar
  4. Bodmer R (1993) The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–729PubMedGoogle Scholar
  5. Blanchard CE (1986) Early development of the thorax and nervous system of the brine shrimp Artemia. Dissertation, University of Leicester, p 68Google Scholar
  6. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, Berlin, p 405Google Scholar
  7. Dalbis A, Pantaloni C, Bechet JJ (1979) Electrophoretic study of native myosin isozymes and of their subunit content. Eur J Biochem 99:261–265CrossRefGoogle Scholar
  8. Daniel RJ (1930a) The abdominal muscles of the shore crab (Carcinus maenas Fabr.) and the zoea and megalopa stages. Proc Trans Liverpool Biol Soc 45:50–56Google Scholar
  9. Daniel RJ (1930b) Comparative study of the abdominal muscles in Malacostraca. Part 1. The main ventral muscles of the typical abdominal segments. Proc Trans Liverp Biol Soc 45:57–71Google Scholar
  10. Daniel RJ (1930c) The abdominal muscular systems of the zoea and mysis stages of the shrimp (Crangon vulgaris Fabr.) and their bearing on phylogeny. Proc Trans Liverpool Biol Soc 44:95–109Google Scholar
  11. Dohle W (1970) Die Bildung und Differenzierung des postnauplialen Keimstreifs von Diastylis rathkei (Crustacea): I Die Bildung der Teloblasten und ihrer Derivate. Z Morphol Tiere 67:307–392CrossRefGoogle Scholar
  12. Dohle W (1972) Über die Bildung und Differenzierung des postnauplialen Keimstreifs von Leptochelia spec. (Crustacea, Tanaidacea). Zool Jb Anat 89:503–566Google Scholar
  13. Fischer A, Scholtz G (2010) Axogenesis in the stomatopod crustacean Gonodactylaceus falcatus (Malacostraca). Invertebr Bio 129:59–76CrossRefGoogle Scholar
  14. Gerberding M, Browne WE, Patel NH (2002) Cell lineage analysis of the amphipod crustacean Parhyale hawaiensis reveals an early restriction of cell fates. Development 129:5789–5801CrossRefPubMedGoogle Scholar
  15. Hartenstein V, Mandal L (2006) The blood/vascular system in a phylogenetic perspective. BioEssays 28:1203–1210CrossRefPubMedGoogle Scholar
  16. Harzsch S, Kreissl S (in press) Myogenesis in the thoracic limbs of the American lobster. Arthr Struct Dev. doi: 10.1016/j.asd.2010.06.001
  17. Hertzler PL, Freas WR (2009) Pleonal muscle development in the shrimp Penaeus (Litopenaeus) vannamei (Crustacea: Malacostraca: Decapoda: Dendrobranchiata). Arthr Struct Dev 38:235–246CrossRefGoogle Scholar
  18. Janssen R, Damen WGM (2008) Diverged and conserved aspects of heart formation in a spider. Evol Dev 10:155–165CrossRefPubMedGoogle Scholar
  19. Kiernan DA, Hertzler PL (2006) Muscle development in dendrobranchiate shrimp, with comparison with Artemia. Evol Dev 8:537–549CrossRefPubMedGoogle Scholar
  20. Kreissl S, Uber A, Harzsch S (2008) Muscle precursor cells in the developing limbs of two isopods (Crustacea, Peracarida): an immunohistochemical study using a novel monoclonal antibody against myosin heavy chain. Dev Genes Evol 218:253–265CrossRefPubMedGoogle Scholar
  21. Oishi S (1959) Studies on the teloblasts in the decapod embryo. 1. Origin of teloblasts in Heptacarpus rectirostris (Stimpson). Embryologica 4:283–309CrossRefGoogle Scholar
  22. Oishi S (1960) Studies on the teloblasts in the decapod embryo. 2. Origin of teloblasts in Pagurus samuelis (Stimpson) and Hemigrapsus sanguineus (de Haan). Embryologica 5:270–282CrossRefGoogle Scholar
  23. Paululat A, Holz A, Renkawitz-Pohl R (1999) Essential genes for myoblast fusion in Drosophila embryogenesis. Mech Dev 83:17–26CrossRefPubMedGoogle Scholar
  24. Price AL, Patel NH (2008) Investigating divergent mechanisms of mesoderm development in arthropods: the expression of Ph-twist and Ph-mef2 in Parhyale hawaiensis. J Exp Zool B Mol Dev Evol 310:24–40CrossRefPubMedGoogle Scholar
  25. Richter S, Scholtz G (2001) Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Res 39:113–136CrossRefGoogle Scholar
  26. Scholtz G (1990) The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peracarida). Proc R Soc Lond 239:163–211CrossRefGoogle Scholar
  27. Scholtz G (1992) Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): germ band formation, segmentation, and early neurogenesis. Roux’s Arch Dev Biol 202:36–48CrossRefGoogle Scholar
  28. Scholtz G (2002) The Articulata hypothesis—or what is a segment? Org Divers Evol 2:197–215CrossRefGoogle Scholar
  29. Scholtz G, Braband A, Tolley L, Reimann A, Mittmann B, Lukhaup C, Steuerwald F, Voigt G (2003) Parthenogenesis in an outsider crayfish. Nature 421:1431–1434CrossRefGoogle Scholar
  30. Seitz R, Vilpoux K, Hopp U, Harzsch S, Maier G (2005) Ontogeny of the Marmorkrebs (marbled crayfish): a parthenogenetic crayfish with unknown origin and phylogenetic position. J Exp Zool 303A:393–405CrossRefGoogle Scholar
  31. Steffens G, Xie F, Kutsch W, Reichert H (1995) Segmental differentiation processes in embryonic muscle development of the grasshopper. Roux's Arch Dev Biol 204:453–464CrossRefGoogle Scholar
  32. Vilpoux K, Sandeman R, Harzsch S (2006) Early embryonic development of the central nervous system in the Australian crayfish and the Marbled crayfish (Marmorkrebs). Dev Genes Evol 216:209–223CrossRefPubMedGoogle Scholar
  33. Vogt G, Tolley L, Scholtz G (2004) Life stages and reproductive components of the Marmorkrebs (marbled crayfish), the first parthenogenetic decapod crustacean. J Morph 261:286–311CrossRefPubMedGoogle Scholar
  34. Weygoldt P (1958) Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex (L.). Zool Jb Anat 77:51–110Google Scholar
  35. Weygoldt P (1961) Beitrag zur Kenntnis der Ontogenie der Dekapoden: Embryologische Untersuchungen. Zool Jb Anat 79:223–270Google Scholar
  36. Wilkens JL, Yazawa T, Cavey MJ (1997) Evolutionary derivation of the American lobster cardiovascular system: an hypothesis based on morphological and physiological evidence. Invertebr Biol 116:30–38CrossRefGoogle Scholar
  37. Wilkens JL (1999) Evolution of the cardiovascular system in Crustacea. Am Zool 39:119–214Google Scholar
  38. Wirkner CS, Richter S (2009a) Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 25:1–25CrossRefGoogle Scholar
  39. Wirkner CS, Richter S (2009b) The circulatory system in malacostraca: evaluating character evolution on the basis of differing phylogenetic hypotheses. Arthr Syst Phyl 67:57–70Google Scholar
  40. Wolff C, Scholtz G (2002) Cell lineage, axis formation and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev Biol 250:44–58CrossRefPubMedGoogle Scholar
  41. Xie F, Garzino V, Herianos S, Meier T, Reichert H (1994) Embryonic expression of muscle-specific antigens in the grasshopper Schistocerca gregaria. Roux's Arch Dev Biol 204:141–145CrossRefGoogle Scholar
  42. Young JH (1959) Morphology of the white shrimp Penaeus setiferus (Linnaeus, 1758). Fishery Bulletin US 59:1–168Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Günther Jirikowski
    • 1
  • Sabine Kreissl
    • 3
  • Stefan Richter
    • 1
  • Carsten Wolff
    • 2
  1. 1.Universität Rostock, Institut für Biowissenschaften/Allgemeine und Spezielle ZoologieRostockGermany
  2. 2.Humboldt-Universität zu Berlin, Institut für Biologie, AG Vergleichende ZoologieBerlinGermany
  3. 3.Universität KonstanzKonstanzGermany

Personalised recommendations