Skip to main content

Advertisement

Log in

Evolution of myogenesis in fish: a sturgeon view of the mechanisms of muscle development

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Patterns of initial muscle formation are well documented for teleost fish. Here, attention is focused upon sturgeons, which arose close to the base of the actinopterygian radiation and whose early development has remained largely unresearched. We demonstrate that some features of muscle development are common to both groups of fish, the most important being the origin and form of migration of adaxial cells to establish the superficial slow fibre layer. This, together with information on initial innervation and capillarisation, strongly suggests a common basis for muscle developmental mechanisms among fish. An important feature that is different between sturgeons and teleosts is that sturgeons lack any cellular dorsal–ventral separation of the myotome that involves the insertion of muscle pioneer (MP)-like cells at the site of the future horizontal septum. This, and information from other fish and from sarcopterygians, permits the supposition that such MP-defined dorsal–ventral separation is a teleost apomorphism. These and other findings are discussed in relation to their significance for the evolution of fish muscle developmental patterns.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen P, Jensen JKS, Løyning Y (1963) Slow and fast muscle fibers in the Atlantic hagfish (Myxine glutinosa). Acta Physiol Scand 57:167–179

    Article  PubMed  CAS  Google Scholar 

  • Bajanca F, Luz M, Duxson MJ, Thorsteinsdóttir S (2004) Integrins in the mouse myotome: developmental changes and differences between the epaxial and hypaxial lineage. Dev Dyn 231:402–415

    Article  PubMed  CAS  Google Scholar 

  • Barresi MJF, Stickney HL, Devoto SH (2000) The zebrafish slow-muscle-omitted gene product is required for hedgehog signal transduction and the development of slow muscle identity. Development 127:2189–2199

    PubMed  CAS  Google Scholar 

  • Bemis WE, Findeis EK, Grande L (1997) An overview of Acipenseriformes. Environ Biol Fish 48:25–71

    Article  Google Scholar 

  • Billard R, Lecointre G (2001) Biology and conservation of sturgeon and paddlefish. Rev Fish Biol Fish 10:355–392

    Article  Google Scholar 

  • Bone Q (1978) Locomotor muscle. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 7. Academic, New York, pp 361–424

  • Chayen N, Rowlerson AM, Squire JM (1993) Fish muscle structure: fibre types in flatfish and mullet fin muscles using histochemistry and antimyosin antibody labelling. J Muscle Res Cell Motil 14:533–542

    Article  PubMed  CAS  Google Scholar 

  • Cheng L, Alvares LE, Ahmed MU, El-Hanfy AS, Dietrich S (2004) The epaxial–hypaxial subdivision of the avian somite. Dev Biol 274:348–369

    Article  PubMed  CAS  Google Scholar 

  • Devoto SH, Melançon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122:3371–3380

    PubMed  CAS  Google Scholar 

  • Devoto SH, Stoiber W, Hammond CL, Steinbacher P, Haslett JR, Barresi MJF, Patterson SE, Adiarte E, Hughes SM (2006) Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol Dev 8:101–110

    Article  PubMed  CAS  Google Scholar 

  • van Eeden FJ, Granato M, Schach U, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg CP, Jiang YJ, Kane DA, Kelsh RN, Mullins MC, Odenthal J, Warga RM, Allende ML, Weinberg ES, Nüsslein-Volhard C (1996) Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123:153–164

    PubMed  Google Scholar 

  • Egginton S (2002) Temperature and angiogenesis: the possible role of mechanical factors in capillary growth. Comp Biochem Physiol A 132:773–787

    Article  Google Scholar 

  • Ekker M, Wegner J, Akimenko MA, Westerfield M (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116:1001–1010

    PubMed  CAS  Google Scholar 

  • Felsenfeld AL, Curry M, Kimmel CB (1991) The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev Biol 148:23–30

    Article  PubMed  CAS  Google Scholar 

  • Flood PR, Gulyaev D, Kryvi H (1987) Origin and differentiation of muscle fibre types in the trunk of the sturgeon, Acipenser stellatus Pallas. Sarsia (Bergen) 72:343–344

    Google Scholar 

  • Gemballa S, Röder K (2004) From head to tail: the myoseptal system in basal actinopterygians. J Morphol 259:155–171

    Article  PubMed  Google Scholar 

  • Gemballa S, Hagen K, Röder K, Rolf M, Treiber K (2003) Structure and evolution of the horizontal septum in vertebrates. J Evol Biol 16:966–975

    Article  PubMed  CAS  Google Scholar 

  • Grimaldi A, Tettamanti G, Martin BL, Gaffield W, Pownall ME, Hughes SM (2004) Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development 131:3249–3262

    Article  PubMed  CAS  Google Scholar 

  • Groves JA, Hammond CL, Hughes SM (2005) Fgf8 drives myogenic progression of a novel lateral fast muscle fibre population in zebrafish. Development 132:4211–4222

    Article  PubMed  CAS  Google Scholar 

  • Hatta K, Bremiller R, Westerfield M, Kimmel CB (1991) Diversity of expression of engrailed-like antigens in zebrafish. Development 112:821–832

    PubMed  CAS  Google Scholar 

  • Hirsinger E, Stellabotte F, Devoto SH, Westerfield M (2004) Hedgehog signaling is required for commitment but not initial induction of slow muscle precursors. Dev Biol 275:143–157

    Article  PubMed  CAS  Google Scholar 

  • Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM (2003) Angiogenic network formation in the developing vertebrate trunk. Development 130:5281–5290

    Article  PubMed  CAS  Google Scholar 

  • Johnston IA, Cole NJ, Vieira VLA, Davidson I (1997) Temperature and developmental plasticity of muscle phenotype in herring larvae. J Exp Biol 200:849–868

    PubMed  Google Scholar 

  • Kahane N, Cinnamon Y, Kalcheim C (1998) The origin and fate of pioneer myotomal cells in the avian embryo. Mech Dev 74:59–73

    Article  PubMed  CAS  Google Scholar 

  • Kielbówna L, Daczewska M (2004) Onto-phylogenetic aspects of myotomal myogenesis in chordata. Folia Biol (Kraków) 52:1–12

    Google Scholar 

  • Killeen JR, McLay HA, Johnston IA (1999) Temperature and neuromuscular development in embryos of the trout (Salmo trutta L.). Comp Biochem Physiol A 122:53–64

    CAS  Google Scholar 

  • Kryvi H, Flood PR, Gulyaev D (1980) The ultrastructure and vascular supply of the different fibre types in the axial muscle of the sturgeon Acipenser stellatus, Pallas. Cell Tissue Res 212:117–126

    Article  PubMed  CAS  Google Scholar 

  • Liem KF, Bemis WE, Walker WF, Grande L (2001) Functional anatomy of the vertebrates, 3rd edn. Harcourt College Publishers, Philadelphia

    Google Scholar 

  • López-Albors O, Gil F, Ramírez-Zarzoza G, Vásquez JM, Latorre R, García-Alcázar A, Arencibia A, Moreno F (1998) Muscle development in the gilthead sea bream (Sparus aurata, L.) and sea bass (Dicentrarchus labrax, L.): further histochemical and ultrastructural aspects. Anat Histol Embryol 27:223–229

    Article  PubMed  Google Scholar 

  • Maurer F (1894) Die Elemente der Rumpfmuskulatur bei Cyclostomen und höheren Wirbelthieren. Morphol Jahrb 21:473–619

    Google Scholar 

  • Melançon E, Liu DW, Westerfield M, Eisen JS (1997) Pathfinding by identified zebrafish motoneurons in the absence of muscle pioneers. J Neurosci 17:7796–7804

    PubMed  Google Scholar 

  • Moody SA, Jacobson M (1983) Compartmental relationships between anuran primary spinal motoneurons and somitic muscle fibers that they first innervate. J Neurosci 3:1670–1682

    PubMed  CAS  Google Scholar 

  • Mos W, Williamson R (1986) A quantitative analysis of the spinal motor pool and its target muscle during growth in the dogfish, Scyliorhinus canicula. J Comp Neurol 248:431–440

    Article  PubMed  CAS  Google Scholar 

  • Myers PZ, Eisen JS, Westerfield M (1986) Development and axonal outgrowth of identified motoneurons in the zebrafish. J Neurosci 6:2278–2289

    PubMed  CAS  Google Scholar 

  • Osborn M, Weber K (1983) Biology of disease tumor diagnosis by intermediate filament typing. Lab Invest 48:372–394

    PubMed  CAS  Google Scholar 

  • Pownall ME, Emerson CP (1992) Sequential activation of three myogenic regulatory genes during somite morphogenesis in quail embryos. Dev Biol 151:67–79

    Article  PubMed  CAS  Google Scholar 

  • Radaelli G, Domeneghini C, Arrighi S, Vaini F, Mascarello F (1999) Histochemical and immunohistochemical investigation of muscle fibres in the sturgeon (Chondrostei; Acipenser). J Appl Ichthyol 15:87–91

    Article  Google Scholar 

  • Rescan P-Y, Collet B, Ralliere C, Cauty C, Delalande J-M, Goldspink G, Fauconneau B (2001) Red and white muscle development in the trout (Oncorhynchus mykiss) as shown by in situ hybridisation of fast an slow myosin heavy chain transcripts. J Exp Biol 204:2097–2101

    PubMed  CAS  Google Scholar 

  • Rowlerson AM, Spurway NC (1988) Histochemical and immunohistochemical properties of skeletal muscle fibres from Rana and Xenopus. Histochem J 20:657–673

    Article  Google Scholar 

  • Roy S, Wolff C, Ingham PW (2001) The u-boot mutation identifies a hedgehog-regulated myogenic switch for fiber-type diversification in the zebrafish embryo. Genes Dev 15:1563–1576

    Article  PubMed  CAS  Google Scholar 

  • Shook DR, Majer C, Keller R (2004) Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev Biol 270:163–185

    Article  PubMed  CAS  Google Scholar 

  • Sive HL, Grainger RM, Harland RM (2000) Whole-mount in situ hybridization. In: Sive HL, Grainger RM, Harland RM (eds) Early development of Xenopus laevis. A laboratory manual. Cold Spring Habor Laboratory Press, New York, pp 249–274

    Google Scholar 

  • Steinbacher P (2004) Patterns of axial muscle formation in actinopterygean fish: a comparative investigation of morphology and expression of muscle specific regulatory genes and structural proteins. Doctoral Thesis, University of Salzburg

  • Stickland NC, White RN, Mescall PE, Crook AR, Thorpe JE (1988) The effect of temperature on myogenesis in embryonic development of the Atlantic salmon (Salmo salar L.). Anat Embryol 178:253–257

    Article  PubMed  CAS  Google Scholar 

  • Stickney HL, Barresi MJF, Devoto SH (2000) Somite development in zebrafish. Dev Dyn 219:287–303

    Article  PubMed  CAS  Google Scholar 

  • Stoiber W (1996) Ontogenesis of axial muscle in teleost fish: an investigation into the source of new muscle fibres and the temperature dependence of growth dynamics. Doctoral Thesis, University of Salzburg

  • Stoiber W, Sänger AM (1996) An electron microscopic investigation into the possible source of new muscle fibres in teleost fish. Anat Embryol 194:569–579

    Article  PubMed  CAS  Google Scholar 

  • Stoiber W, Haslett JR, Goldschmid A, Sänger AM (1998) Patterns of superficial fibre formation in the European pearlfish (Rutilus frisii meidingeri) provide a general template for slow muscle development in teleost fish. Anat Embryol 197:485–496

    Article  PubMed  CAS  Google Scholar 

  • Stoiber W, Haslett JR, Wenk R, Steinbacher P, Gollmann H-P, Sänger AM (2002a) Cellularity changes in developing red and white fish muscle at different temperatures: simulating natural environment conditions for a temperate freshwater cyprinid. J Exp Biol 205:2349–2364

    PubMed  Google Scholar 

  • Stoiber W, Haslett JR, Steinbacher P, Freimüller M, Sänger AM (2002b) Tonic fibres in axial muscle of cyprinid fish larvae: their definition, possible origins and functional importance. Anat Embryol 205:113–124

    Article  PubMed  CAS  Google Scholar 

  • Sunier ALJ (1911) Les premiers stades de la différentiation interne du myotome et la formation des éléments sclérotomatiques chez les acraniens, les sélaciens, et les téléostéens. Tijdschr Ned Dierkundige Vereenig 12:75–181

    Google Scholar 

  • Vieira VLA, Johnston IA (1996) Muscle development in the tambaqui, an important Amazonian food fish. J Fish Biol 49:842–853

    Article  Google Scholar 

  • Vieira VLA, Johnston IA (1999) Temperature and neuromuscular development in the tambaqui. J Fish Biol 55(Suppl A):66–83

    Article  Google Scholar 

  • Waterman RE (1969) Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. Am J Anat 125:457–497

    Article  PubMed  CAS  Google Scholar 

  • Westneat MW, Wainwright SA (2001) Mechanical design for swimming: muscle, tendon, and bone. In: Block BA, Stevens ED (eds) Tuna. Physiology, ecology and evolution. Fish physiology, vol 19. Academic, San Diego, pp 271–311

  • Wilkinson DG (1992) Whole mount in situ hybridization of vertebrate embryos. In: Wilkinson DG (ed) In situ hybridization: a practical approach. Oxford University Press, Oxford, pp 75–83

    Google Scholar 

  • Wolff C, Roy S, Ingham PW (2003) Multiple muscle cell identities induced by distinct levels and timing of hedgehog activity in the zebrafish embryo. Curr Biol 13:1169–1181

    Article  PubMed  CAS  Google Scholar 

  • Zeller J, Granato M (1999) The zebrafish diwanka gene controls an early step of motor growth cone migration. Development 126:3461–3472

    PubMed  CAS  Google Scholar 

  • Zeller J, Schneider V, Malayaman S, Higashijima S, Okamoto S, Gui J, Lin S, Granato M (2002) Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev Biol 252:241–256

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Granato M (2000) The zebrafish unplugged gene controls motor axon pathway selection. Development 127:2099–2111

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Hans Bergler, Wöllershof Hatchery, Störnstein, Germany, for providing the sturgeon fry; Pierre-Yves Rescan, INRA Rennes, France, for providing MyHCs cDNA; and Anthea Rowlerson, University of London, UK, for the supply of antibodies. Sincere thanks also to Malgorzata Daczewska of the University of Wroclaw, Poland, for the many fruitful discussions in relation to sturgeon development. Hans-Peter Gollmann (Institute of Water Ecology, Fisheries Biology and Lake Research, Scharfling, Austria) together with Adda Maenhardt, Synnoeve Tholo and Andreas Zankl (all University of Salzburg, Austria) provided excellent technical support. The work was supported by Austrian Science Foundation (FWF) grants P16425 and P14193.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Steinbacher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Steinbacher, P., Haslett, J.R., Sänger, A.M. et al. Evolution of myogenesis in fish: a sturgeon view of the mechanisms of muscle development. Anat Embryol 211, 311–322 (2006). https://doi.org/10.1007/s00429-006-0082-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-006-0082-4

Keywords

Navigation