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Developmental Patterning and Evolution of the Mammalian Viscerocranium: Genetic Insights Into Comparative Morphology

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Developmental Patterning and Evolution of the Mammalian Viscerocranium: Genetic Insights Into Comparative Morphology DEVELOPMENTAL DYNAMICS 209:139–155 (1997) REVIEW ARTICLE Developmental Patterning and Evolution of the Mammalian Viscerocranium: Genetic Insights Into Comparative Morphology SHIGERU KURATANI,* ISAO MATSUO, AND SHINICHI AIZAWA Department of Morphogenesis, Institute of Molecular Embryology and Genetics, Kumamoto University School of Medicine, Kumamoto 860, Japan ABSTRACT The vertebrate cranium is gen- rally bound to its segmental plan and its evolutionary erally classified into the neurocranium and the origin. The concept of segmental vertebrate head stems viscerocranium. The latter is derived from the from Goethe (1790), Oken (1807), and Owen (1866) who neural crest and so is the prechordal portion of speculated that the vertebrate skull was composed of a the neurocranium. A view we favor considers the certain number of fused vertebrae (Fig. 1A). This view prechordal neurocranium as the premandibular is now accepted only in the occipital region that arises component of the viscerocranium, and the verte- from somites (reviewed by Noden, 1988; Couly et al., brate skull to consist of the neural crest-derived 1993), but the basic concepts of the metamerism and viscerocranium and the mesodermal neurocra- metamorphosis of the cranium are still valid in the nium. Of these developmental units, only the pharyngeal portion of the skull since branchial arch viscerocranium appears to have completely seg- cartilages are also repeating units along the anteropos- mented metamerical organization. The Hox code terior axis. which is known to function in specification of the Anatomically, the vertebrate cranium is divided into viscerocranium does not extend rostrally into the the brain case (neurocranium) and the pharyngeal arch mandibular and premandibular segments. By ge- skeletons (viscerocranium; Fig. 1B; see e.g., Portmann, netic manipulation of rostrally expressed non- 1976; and Torrey and Feduccia, 1979). These neuro- Hox homeobox genes, the patterning mechanism and viscerocrania contain cartilaginous elements com- of the head is now demonstrated to be more prising the chondrocranium. The dermal exoskeleton complicated than isomorphic registration of the covers the entire chondrocranium as dermatocranium Hox code to pharyngeal arches. The phenotype by and is also divided dorsoventrally into neuro- and haplo-insufficiency of Otx2 gene, in particular, viscerocranial elements. The neurocranium is regarded implies the premandibular cranium shares a com- as the rostral continuation of the vertebral column mon specification mechanism with the mandibu- containing the central nervous system. To this the lar arch. Our interpretation of the metamerical cartilaginous sensory capsules, the nasal, optic, and plan of the viscerocranium offers a new scheme otic capsules are attached. The main portion of the of molecular codes associated with the verte- neurocranium is the sphenoid bone and the dermal brate head evolution. Dev. Dyn. 209:139–155, calvarium, and the caudal portion is the occipital, which is thought to be the secondarily attached verte- 1997. 1997 Wiley-Liss, Inc. r brae (Fig. 1B; Fu¨ rbringer, 1897; reviewed by de Beer, 1937; Goodrich, 1930). The viscerocranium is composed Key words: cranium; homeobox genes; pharyn- of a series of repeated bar-like cartilages within the geal arch; mandibular arch; tra- pharyngeal arches. The rostral-most element is called becula; comparative embryology; evo- the mandibular arch skeleton and is altered to function lution as upper and lower jaws in gnathostomes. Experimental embryology has revealed that the ver- tebrate head contains two types of mesenchyme as the INTRODUCTION Morphological and Developmental View of the Vertebrate Cranium The cranium comprises the most complicated part of *Correspondence to: Shigeru Kuratani, Department of Morphogen- the vertebrate body and has long stimulated questions esis, Institute of Molecular Embryology and Genetics, Kumamoto University School of Medicine, 4-24-1, Kuhonji, Kumamoto, Kuma- as to how this structure is constructed and how it moto 860, Japan. E-mail: [email protected] develops during ontogeny. These questions are natu- Received 26 September 1996; Accepted 25 February 1997 r 1997 WILEY-LISS, INC. A eye inner ear nasal organ orbital otic B neurocranium region capsule nasal capsule notocord pharynx dermocranium mandibular hyoid gill arch arch arches viscerocranium C orbital cartilage nasal capsule otic capsule quadrate cartilage occipital cartilage vertebrae trabecula Meckel's cartilage hyoid arch parachordal cartilage branchial arches notocord Fig. 1. Morphological plans of the cranium. A: Idealistic vertebrate as changed into the jaw. Sensory capsules are attached to the neurocra- segmental organism, redrawn from Owen (1866). B: Generally accepted nium. These cranial elements are cartilaginous and the whole chondrocra- architecture of the vertebrate cranium, redrawn from Torrey and Feduccia nium is covered by dermal elements, the dermatocranium. Note the (1979). The skull of gnathostomes consists of neurocranium, viscerocra- caudal portion of the neurocranium is actually the fused vertebrae, the nium, and dermatocranium. The neurocranium contains the brain inside occipital. C: Early embryonic chondrocranium of a lizard, redrawn from and the viscerocranium covers the pharynx. The latter further consists of Torrey and Feduccia (1979). Note the position of prechordal cartilage, or metamerical series of cartilage bars of which the rostralmost element is the trabecula. MORPHOGENESIS OF THE MAMMALIAN SKULL 141 source of the cranium, i.e., the neural crest-derived belongs to the same segment as the ophthalmic nerve, ectomesenchyme and mesoderm. Mesodermal mesen- as was first stated by Huxley (1874; reviewed by chyme is dorsally located as cranial paraxial mesoderm Goodrich, 1930; de Beer, 1931, 1937; also see Stad- lateral to the neural tube, and ventrally, the ectomesen- mu¨ ller, 1936). Although several arguments exist, we chyme resides in the pharyngeal arches thereby form- favor this view based on the recent genetic data stated ing pharyngeal arch skeletons (reviewed by Noden, below. 1988; Ko¨ntges and Lumsden, 1996; Couly et al., 1996). Considering an ammocoete larva of the lamprey as a Thus, all the viscerocranial elements (both cartilagi- hypothetical intermediate state, de Beer (1931) viewed nous and dermal) are of neural crest-origin (Le Lie`vre the mucocartilage in the upper lip as the trabecula and Le Douarin, 1975; reviewed by Noden, 1988; Couly homologue and tried to explain how the premandibu- et al., 1993). larly located branchial cartilage could have moved into Comparative embryology can, to some degree, predict the position of the prechordal neurocranium. He as- mesenchymal origins of mammalian cranial elements sumed a great change in the topographical relationship (see Fig. 2B). The origin of dermal bones in the cal- between the neural tube and the cartilaginous compo- varium still remains a matter of controversy (Le Lie`vre, nent to explain how the trabecula had come into contact 1978; Noden, 1988; Couly et al., 1993). As for the origin with the nasal epithelium, hypophysis, and the fore- of laryngeal cartilages in amniotes, Gegenbaur (1898; brain. The common anatomical plan of the rostral-most also see Starck, 1979) assumed their homologies with neural tube is shared by a closely related group of caudal branchial arch cartilages, which seems unlikely. vertebrates, the amphioxus (Lacalli et al., 1994); it is It has been shown in avian embryos that these carti- hardly conceivable that such a substantial change took lages including tracheal rings are derived from the place in the gnathostome evolution. Instead, Holmgren lateral mesoderm; they are more likely to represent and Stensio¨ (1936) and others identified the ammocoete neomorphic structures (Noden, 1983b). In the mamma- trabecula as the cartilage that develops as the rostral lian cranium, therefore, the caudalmost pharyngeal continuation of the parachordal, not the mucocartilage arch cartilage appears to be the caudal part of the hyoid juxtaposed to the mandibula. The mucocartilage that body that belongs to the arch 3 region. de Beer (1931) called the trabecula does not seem to arise from the neural crest either (reviewed by Janvier, On the Trabecula Cranii 1993). The mesodermal mesenchyme does not exist rostrally The ectomesenchyme forming the trabecula may beyond the level of the hypophysis; the notochord, have been originally located in close association with which is essential for chondrogenesis of mesodermal the rostral-most part of the gut (Allis, 1938), similar to tissue, also does not exist in this area (Pourquie et al., what is the case for the other pharyngeal arch skeletal 1993). Data obtained in avian experiments confirmed elements. In most of the early vertebrate embryos, the that the prechordal neurocranium originates from the rostral-most portion of the gut is seen as the preoral gut neural crest (Le Lie`vre and Le Douarin, 1975; reviewed located dorsoanterior to the mouth. The vertebrate by Noden, 1988; Couly et al., 1993). In mammalian mouth is formed in the ventral aspect of the pharynx skulls, nasal septum, lachrymal, presphenoid, basisphe- and caudal to the trabecular mesenchyme (Fig. 3A). noid (in part?), and anterior portions of orbitosphenoid The position of the preoral gut is very close to the and frontal bones are thought to belong to the pre- hypophysis, nasal epithelium, forebrain, and the oph- chordal region; a part of the frontal bone may also be thalmic
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