Skip to main content
SpringerLink
Log in

Somite compartments in anamniotes

  • Review
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Somites are a common feature of the phylotypic stage of embryos of all higher chordates. In amniote species like mouse and chick, somite development has been the subject of intense research over many decades, giving insight into the morphological and molecular processes leading to somite compartmentalization and subsequent differentiation. In anamniotes, somite development is much less understood. Except for recent data from zebrafish, and morphological studies in Xenopus, very little is known about the formation of somite compartments and the differentiation of somite derivatives in anamniotes. Here, we give a brief overview on the development of myotome, sclerotome and dermomyotome in various anamniote organisms, and point out the different mechanisms of somite development between anamniotes and the established amniote model systems.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Balfour FM (1878) Development of elasmobranch fishes. Macmillan, London

    Google Scholar 

  • Blagden CS, Currie PD, Ingham PW, Hughes SM (1997) Notochord induction of zebrafish slow muscle mediated by Sonic hedgehog. Genes Dev 11:2163–2175

    Article  PubMed  CAS  Google Scholar 

  • Bone Q (1989) Evolutionary patterns of axial muscle systems in some invertebrates and fish. Am Zool 29:5–18

    Google Scholar 

  • Boudjelida H, Muntz L (1987) Multinucleation during myogenesis of the myotome of Xenopus laevis: a qualitative study. Development 101:583–590

    PubMed  CAS  Google Scholar 

  • Brand-Saberi B, Christ B (2000) Evolution and development of distinct cell lineages derived from somites. Curr Top Dev Biol 48:1–42

    Article  PubMed  CAS  Google Scholar 

  • Brennan C, Amacher SL, Currie PD (2002) Somitogenesis. Results Probl Cell Differ 40:271–297

    PubMed  CAS  Google Scholar 

  • Brustis J-J, Landsmann F, Gipouloux J-D (1976) Etude de la differenciation des somiteschez les embryons de deux amphibiens Anoures: Crapaud commun (Bufo bufo) et Grenouille agile (Rana dalmatina). Bull Biol Fr Belg 110 (3):299–311

    PubMed  CAS  Google Scholar 

  • Brustis J-J (1978) Organisation precoce du dermatome et du sclerotome chez deux amphibiens anoures Rana dalmatina et Bufo bufo. C R Acad Sci Paris 287:1153–1155

    CAS  Google Scholar 

  • Bush JO, Maltby KM, Cho ES, Jiang R (2003) The T-box gene Tbx10 exhibits a uniquely restricted expression pattern during mouse embryogenesis. Gene Expr Patterns 3:533–538

    Article  PubMed  CAS  Google Scholar 

  • Chieffo C, Garvey N, Gong W, Roe B, Zhang G, Silver L, Emanuel BS, Budarf ML (1997) Isolation and characterization of a gene from the DiGeorge chromosomal region homologous to the mouse Tbx1 gene. Genomics 43:267–277

    Article  PubMed  CAS  Google Scholar 

  • Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol (Berl) 191:381–396

    Article  CAS  Google Scholar 

  • Christ B, Huang R, Scaal M (2004) Formation and differentiation of the avian sclerotome. Anat Embryol (Berl) 208:333–350

    Google Scholar 

  • Coutelle O, Blagden CS, Hampson R, Halai C, Rigby PW, Hughes SM (2001) Hedgehog signalling is required for maintenance of myf5 and myoD expression and timely terminal differentiation in zebrafish adaxial myogenesis. Dev Biol 236:136–150

    Article  PubMed  CAS  Google Scholar 

  • Daczewska M, Saczko J (2005) Myotomal myogenesis of axial muscle in the sturgeon Acipenser baeri (Chondrostei, Acipenseriformes). Folia Biol (Krakow) 53:29–38

    Article  Google Scholar 

  • Devoto SH, Melancon 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 MJ, Patterson SE, Adiarte EG, Hughes SM (2006) Generality of vertebrate developmental patterns: evidence for a dermomyotome in fish. Evol Dev 8:101–110

    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. Sarsia 72:343–344

    Google Scholar 

  • Freitas R, Zhang G, Cohn MJ (2006) Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442(7106):1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Geetha-Loganathan P, Nimmagadda S, Huang R, Christ B, Scaal M (2006) Regulation of ectodermal Wnt6 expression by the neural tube is transduced by dermomyotomal Wnt11: a mechanism of dermomyotomal lip sustainment. Development 133:2897–2904

    Article  PubMed  CAS  Google Scholar 

  • Gossler A, Hrabe de Angelis M (1998) Somitogenesis. Curr Top Dev Biol 38:225–287

    Article  PubMed  CAS  Google Scholar 

  • Grenacher H (1867) Beiträge zur näheren Kenntnis der Muskulatur der Cyklostomen und Leptokardier. Zeitschr. f. wissensch. Zool. 17

  • 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 

  • Gros J, Scaal M, Marcelle C (2004) A two-step mechanism for myotome formation in chick. Dev Cell 6:875–882

    Article  PubMed  CAS  Google Scholar 

  • Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435:954–958

    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 

  • Hamilton L (1969) The formation of somites in Xenopus. J Embryol Exp Morphol 22:253–264

    PubMed  CAS  Google Scholar 

  • Hatschek B (1888) Ueber den Schichtenbau des Amphioxus. Anat Anz

  • Hatschek B (1892) Die Metamerie des Amphioxus und des Ammocoetes. Verhandl d Anat Ges Wien 6:136–162

    Google Scholar 

  • Henry CA, Amacher SL (2004) Zebrafish slow muscle cell migration induces a wave of fast muscle morphogenesis. Dev Cell 7:917–923

    Article  PubMed  CAS  Google Scholar 

  • Hertwig O (1898) Lehrbuch der Entwicklungsgeschichte des Menschen und der Wirbelthiere. Gustav Fischer, Jena

  • 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 

  • Holland ND, Holland LZ, Kozmik Z (1995a) An amphioxus Pax gene, AmphiPax-1, expressed in embryonic endoderm, but not in mesoderm: implications for the evolution of class I paired box genes. Mol Mar Biol Biotechnol 4:206–214

    CAS  Google Scholar 

  • Holland LZ, Pace DA, Blink ML, Kene M, Holland ND (1995b) Sequence and expression of amphioxus alkali myosin light chain (AmphiMLC-alk) throughout development: implications for vertebrate myogenesis. Dev Biol 171:665–676

    Article  CAS  Google Scholar 

  • Holland LZ, Schubert M, Kozmik Z, Holland ND (1999) AmphiPax3/7, an amphioxus paired box gene: insights into chordate myogenesis, neurogenesis, and the possible evolutionary precursor of definitive vertebrate neural crest. Evol Dev 1:153–165

    Article  PubMed  CAS  Google Scholar 

  • Holley SA, Nusslein-Volhard C (2000) Somitogenesis in zebrafish. Curr Top Dev Biol 47:247–277

    Article  PubMed  CAS  Google Scholar 

  • Huang R, Zhi Q, Wilting J, Christ B (1994) The fate of somitocoele cells in avian embryos. Anat Embryol (Berl) 190:243–250

    CAS  Google Scholar 

  • Huang R, Zhi Q, Neubuser A, Muller TS, Brand-Saberi B, Christ B, Wilting J (1996) Function of somite and somitocoele cells in the formation of the vertebral motion segment in avian embryos. Acta Anat (Basel) 155:231–241

    Article  CAS  Google Scholar 

  • Kästner A (1892) Über die allgemeine Bildung der Rumpf und Schwanzmuskulatur. Arch f Anat u Physiol Abt Anat

  • Kästner A (1893) Die Entwicklung der Extremitäten- und Bauchmuskulatur bei den anuren Amphibien. Arch f Anat u Physiol Abt Anat

  • Keller R (2000) The origin and morphogenesis of amphibian somites. Curr Top Dev Biol 47:183–246

    Article  PubMed  CAS  Google Scholar 

  • Kerr JG (1909) Normal plates of the development of Lepidosiren paradoxa and Protopterus annectens. In: F. K, editor. Normentafeln zur Entwicklungsgeschichte der Wirbeltiere. Jena, Gustav Fischer

  • Kielbowna L (1966) Cytological and cytophotometrical studies on myogenesis in Xenopus laevis. Zool Pol 11:247–255

    Google Scholar 

  • Kielbowna L, Koscielski B (1979) Myotomal myogenesis in Bombina variegata. Roux’s Arch Dev Biol 185:295–303

    CAS  Google Scholar 

  • Kielbowna L (1980) Two different types of myogenesis in Xenopus laevis. Zool Pol 27

  • Kielbowna L (1981) The formation of somites and early myotomal myogenesis in Xenopus laevis, Bombina variegata and Pelobates fuscus. J Embryol Exp Morphol 64:295–304

    PubMed  CAS  Google Scholar 

  • Kitchen IC (1949) The effects of notochordectomy in Ambystoma mexicanum. J Exp Zool 112:393–411

    Article  Google Scholar 

  • Kusakabe R, Kuratani S (2005) Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Dev Dyn 234:824–834

    Article  PubMed  Google Scholar 

  • Lacalli TCK, Kelly SJ (1999) Somatic motoneurons in amphioxus larvae: cell types, cell position and innervation patterns. Acta Zool. 80:113–124

    Article  Google Scholar 

  • Le Guellec D, Morvan-Dubois G, Sire JY (2004) Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). Int J Dev Biol 48:217–231

    Article  PubMed  CAS  Google Scholar 

  • Mahadevan NR, Horton AC, Gibson-Brown JJ (2004) Developmental expression of the amphioxus Tbx1/ 10 gene illuminates the evolution of vertebrate branchial arches and sclerotome. Dev Genes Evol 214:559–566

    Article  PubMed  CAS  Google Scholar 

  • Marcelle C, Lesbros C, Linker C (2002) Somite patterning: a few more pieces of the puzzle. Results Probl Cell Differ 38:81–108

    PubMed  Google Scholar 

  • Mauger A (1972) Role du mesoderme somitique dans le developpement du plumage dorsal chez l’embryon du poulet. I. Origine, capacites de regulation et determination du mesoderme plumigene. J Embryol Exp Morphol 28:313–341

    PubMed  CAS  Google Scholar 

  • Maurer F (1894) Die Elemente der Rumpfmuskulatur bei Cyklostomen und höheren Wirbeltieren, ein Beitrag zur Phylogenie der quergestreiften Muskelfaser. Morph. Jahrb. 21

  • Maurer F (1906) Die Entwickelung des Muskelsystems und der elektrischen Organe. In: Hertwig O (ed) Handbuch der vergleichenden und experimentellen Entwickelungslehre der Wirbeltiere. Gustav Fischer, Jena

    Google Scholar 

  • Meedel TH, Crowther RJ, Whittaker JR (1987) Determinative properties of muscle lineages in ascidian embryos. Development 100:245–260

    PubMed  CAS  Google Scholar 

  • Mittapalli VR, Huang R, Patel K, Christ B, Scaal M (2005) Arthrotome: a specific joint forming compartment in the avian somite. Dev Dyn 234:48–53

    Article  PubMed  Google Scholar 

  • Mookerjee HK (1930) On the development of the vertebral column of Urodela. Philos Trans R Soc London Ser B 218:415–446

    Article  Google Scholar 

  • Mookerjee HK (1931) On the development of the vertebral column of Anura. Philos Trans R Soc London Ser B 219:165–196

    Article  Google Scholar 

  • Morin-Kensicki EM, Eisen JS (1997) Sclerotome development and peripheral nervous system segmentation in embryonic zebrafish. Development 124:159–167

    PubMed  CAS  Google Scholar 

  • Muntz L (1975) Myogenesis in the trunk and leg during development of the tadpole of Xenopus laevis (Daudin 1802). J Embryol Exp Morphol 33:757–774

    PubMed  CAS  Google Scholar 

  • Neff AW, Malacinski GM, Chung HM (1989) Amphibian (urodele) myotomes display transitory anterior/posterior and medial/lateral differentiation patterns. Dev Biol 132:529–543

    Article  PubMed  CAS  Google Scholar 

  • Neyt C, Jagla K, Thisse C, Thisse B, Haines L, Currie PD (2000) Evolutionary origins of vertebrate appendicular muscle. Nature 408:82–86

    Article  PubMed  CAS  Google Scholar 

  • Nishida H (1990) Determinative mechanisms in secondary muscle lineages of ascidian embryos: development of muscle-specific features in isolated muscle progenitor cells. Development 108:559–568

    PubMed  CAS  Google Scholar 

  • Nornes S, Mikkola I, Krauss S, Delghandi M, Perander M, Johansen T (1996) Zebrafish Pax9 encodes two proteins with distinct C-terminal transactivating domains of different potency negatively regulated by adjacent N-terminal sequences. J Biol Chem 271:26914–26923

    Article  PubMed  CAS  Google Scholar 

  • Rabl C (1888) Über die Differenzierung des Mesoderms. Verh d Anat Ges Würzburg

  • Rabl C (1889) Theorie des Mesoderms. I u.II. Teil. Morph. Jahrb. 15, 19

  • Rescan PY, Ralliere C, Chauvigne F, Cauty C (2005) Expression patterns of collagen I (alpha1) encoding gene and muscle-specific genes reveal that the lateral domain of the fish somite forms a connective tissue surrounding the myotome. Dev Dyn 233:605–611

    Article  PubMed  CAS  Google Scholar 

  • Ruppert EE (1997) Cephalochordata (Acrania). In: Harrison FW, Ruppert EE (eds) Microscopic anatomy of investebrates, vol. 15. Wiley, New York, pp 349–504

  • Ryke PAI (1953) The ontogenesis development of the somatic musculature of the trunk of the aglossa anuran Xenopus laevis (Daudin). Acta Zool 34:1–70

    Article  Google Scholar 

  • Satoh N, Jeffery WR (1995) Chasing tails in ascidians: developmental insights into the origin and evolution of chordates. Trends Genet 11:354–359

    Article  PubMed  CAS  Google Scholar 

  • Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl) 208:411–424

    Google Scholar 

  • Scammon RE (1911) Normal plates of the development of Squalus acanthias. In: Keibel F (ed) Normentafeln zur Entwicklungsgeschichte der Wirbeltiere. Gustav Fischer, Jena

    Google Scholar 

  • Schmidt W (1992) The amniotic fluid compartment: the fetal habitat. Adv Anat Embryol Cell Biol 127:1–100

    PubMed  CAS  Google Scholar 

  • Schubert M, Holland LZ, Stokes MD, Holland ND (2001) Three amphioxus Wnt genes (AmphiWnt3, AmphiWnt5, and AmphiWnt6) associated with the tail bud: the evolution of somitogenesis in chordates. Dev Biol 240:262–273

    Article  PubMed  CAS  Google Scholar 

  • Semon R (1901) Normentafel zur Entwicklungsgeschichte des Ceratodus fosteri. In: Keibel F (ed) Normentafeln zur Entwicklungsgeschichte der Wirbeltiere. Gustav Fischer, Jena

    Google Scholar 

  • Shimeld SM, Holland PW (2000) Vertebrate innovations. Proc Natl Acad Sci USA 97:4449–4452

    Article  PubMed  CAS  Google Scholar 

  • Steinbacher P, Haslett JR, Sanger AM, Stoiber W (2006) Evolution of myogenesis in fish: a sturgeon view of the mechanisms of muscle development. Anat Embryol (Berl) 211:311–322

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Stoiber W, Haslett JR, Goldschmid A, Sanger 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 (Berl) 197:485–496

    Article  CAS  Google Scholar 

  • Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203–1215

    PubMed  CAS  Google Scholar 

  • van Wijhe JW (1889) Über die Mesodermsegmente des Rumpfes und die Entwicklung des Exkretionssystems bei Selachiern. Arch f mikr Anat 33

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

    Article  Google Scholar 

  • Wake D (1970) Aspects of vertebral evolution in the modern amphibia. Forma et Functio 3:33–60

    Google Scholar 

  • Wake M, Wake D (1985) Vertebral development in gymnophion amphibians: resegmentation and homology. Am Zool 25:93a

    Google Scholar 

  • Waterman RE (1969) Development of the lateral musculature in the teleost, Brachydanio rerio: a fine structural study. Am J Anat 125:457–493

    Article  PubMed  CAS  Google Scholar 

  • Weinberg ES, Allende ML, Kelly CS, Abdelhamid A, Murakami T, Andermann P, Doerre OG, Grunwald DJ, Riggleman B (1996) Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122:271–280

    PubMed  CAS  Google Scholar 

  • Wilson P, Keller R (1991) Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. Development 112:289–300

    PubMed  CAS  Google Scholar 

  • Youn BW, Malacinski GM (1981a) Comparative analysis of amphibian somite morphogenesis: cell rearrangement patterns during rosette formation and myoblast fusion. J Embryol Exp Morphol 66:1–26

    CAS  Google Scholar 

  • Youn BW, Malacinski GM (1981b) Somitogenesis in the amphibian Xenopus laevis: scanning electron microscopic analysis of intrasomitic cellular arrangements during somite rotation. J Embryol Exp Morphol 64:23–43

    CAS  Google Scholar 

  • Zeller J, Schneider V, Malayaman S, Higashijima S, Okamoto H, 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 

Download references

Acknowledgments

We thank Drs. Shigeru Kuratani and Thurston Lacalli for valuable hints on the literature. We are greatly indebted to Drs. Rie Kusakabe, Thurston Lacalli, and Walter Stoiber for generously providing unpublished photographic material. This work was supported by the Deutsche Forschungsgemeinschaft (SFB592 and GRK1104 to M.S.) and the European Network of Excellence MYORES to M.S.

Author information

Authors and Affiliations

  1. Institute of Anatomy and Cell Biology, Department of Molecular Embryology, University of Freiburg, Albertstrasse 17, 79104, Freiburg, Germany

    Martin Scaal & Christoph Wiegreffe

Authors
  1. Martin Scaal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christoph Wiegreffe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Scaal.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scaal, M., Wiegreffe, C. Somite compartments in anamniotes. Brain Struct Funct 211 (Suppl 1), 9–19 (2006). https://doi.org/10.1007/s00429-006-0127-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-006-0127-8

Keywords

Search

Navigation