Developmental fate of the mandibular mesoderm in the lamprey, Lethenteron japonicum: Comparative morphology and development of the gnathostome jaw with special reference to the nature of the trabecula cranii

Authors

  • Shigeru Kuratani,

    Corresponding author
    1. Laboratory for Evolutionary Morphology, Center for Developmental Biology, RIKEN, Kobe, Hyogo 650-0047, Japan
    • Laboratory for Evolutionary Morphology, Center for Developmental Biology, RIKEN 2-2-3 Minatojima-minami, Chuo Kobe, Hyogo 650-0047, Japan
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  • Yasunori Murakami,

    1. Laboratory for Evolutionary Morphology, Center for Developmental Biology, RIKEN, Kobe, Hyogo 650-0047, Japan
    Current affiliation:
    1. Institut de Genetique et de Biologie Moleculaire et Cellulaire (IGBMC), CNRS/INSERM/ULP, CU de Strasbourg, BP 10142-67404 Illkirch Cedex, France
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  • Yoshiaki Nobusada,

    1. Department of Biology, Okayama University, Okayama 700-8530, Japan
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  • Rie Kusakabe,

    1. Laboratory for Evolutionary Morphology, Center for Developmental Biology, RIKEN, Kobe, Hyogo 650-0047, Japan
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  • Shigeki Hirano

    1. Department of Medical Technology, School of Health Sciences, Faculty of Medicine, Niigata University, 2-746, Asahimachi, Niigata 951-8518, Japan
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Abstract

The vertebrate jaw is a mandibular-arch derivative, and is regarded as the synapomorphy that defines the gnathostomes. Previous studies (Kuratani et al., Phil. Trans. Roy. Soc. 356:15, 2001; Shigetani et al., Science 296:1319, 2002) have suggested that the oral apparatus of the lamprey is derived from both the mandibular and premandibular regions, and that the jaw has arisen as a secondary narrowing of the oral patterning mechanism into the mandibular-arch domain. The heterotopy theory of jaw evolution states that the lamprey upper lip is a premandibular element, leaving further questions unanswered as to the homology of the trabecula in the lamprey and gnathostomes, and to the morphological nature of the muscles in the upper lip. Using focal injection of vital dyes into the cheek process core of lamprey embryos, we found that the upper lip muscle and trabecula are both derived from mandibular mesoderm. Secondary movement of the muscle primordium is also evident when the expression of the early muscle marker gene, LjMA2, is visualized. A nerve-fiber labeling study revealed that the upper lip muscle-innervating neurons are located in the rostral part of the brain stem, where the trigeminal motor nuclei are not found in gnathostomes. We conclude that the lamprey upper lip is composed of premandibular ectomesenchyme and a lamprey-specific muscle component derived from the mandibular mesoderm innervated by lamprey-specific motoneurons. Furthermore, the lamprey trabecula is most likely equivalent to a mesodermally derived neurocranial element, similar to the parachordal element in gnathostomes, rather than to the neural-crest-derived prechordal element. J. Exp. Zool. (Mol. Dev. Evol.) 302B:000–000, 2004. © 2004 Wiley-Liss, Inc.

Ancillary