Evolutionary origins of vertebrate appendicular muscle

Abstract

The evolution of terrestrial tetrapod species heralded a transition in locomotor strategies. While most fish species use the undulating contractions of the axial musculature to generate propulsive force, tetrapods also rely on the appendicular muscles of the limbs to generate movement1,2. Despite the fossil record generating an understanding of the way in which the appendicular skeleton has evolved to provide the scaffold for tetrapod limb musculature3, there is, by contrast, almost no information as to how this musculature arose. Here we examine fin muscle formation within two extant classes of fish. We find that in the teleost, zebrafish, fin muscles arise from migratory mesenchymal precursor cells that possess molecular and morphogenetic identity with the limb muscle precursors of tetrapod species. Chondrichthyan dogfish embryos, however, use the primitive mechanism of direct epithelial somitic extensions to derive the muscles of the fin. We conclude that the genetic mechanism controlling formation of tetrapod limb muscles evolved before the Sarcopterygian radiation.

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Figure 1: Zebrafish fin muscle formation.
Figure 2: Identification of fin muscle precursors within zebrafish somites.
Figure 3: Expression of zebrafish lbx1 and mox genes.
Figure 4: Fin muscle formation in S. canicula.

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Acknowledgements

We are indebted to B. Mankoo for his gift of the zebrafish mox clone and for sharing results before publication. We also thank S. Hughes and M. Goulding for antibodies; and M. Buckingham, R. Sporle, N. Rosenthal, N. Hastie, R. Currie and members of the Currie lab for discussion and critical reading of the manuscript. We thank the staff at the University of Glasgow's Milport Marine Station, Isle of Cumbrae, for the supply of S. canicula embryos; T. Chapman and J. Mattocks for animal husbandry; and P. Perry for help with microscopy. K.J. was supported by grants from the Human Frontier Science Program and from the Association Francaise contre les Myopathies (AFM). C.T. and B.T. were supported by funds from the Institut National de la Santé et de la Recherche Médicale, the Centre National de la Recherche Scientifique, the Hopital Universitaire de Strasbourg, the Association de Recherche sur le Cancer and the Ligue Nationale Contre le Cancer. P.D.C. is supported by a MRC career development fellowship and the BBSRC.

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Correspondence to P. D. Currie.

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