Developmental Morphology of the Head Mesoderm and Reevaluation of Segmental Theories of the Vertebrate Head: Evidence from Embryos of an Agnathan Vertebrate, Lampetra japonica

Abstract

Due to the peculiar morphology of its preotic head, lampreys have long been treated as an intermediate animal which links amphioxus and gnathostomes. To reevaluate the segmental theory of classical comparative embryology, mesodermal development was observed in embryos of a lamprey, Lampetra japonica, by scanning electron microscopy and immunohistochemistry. Signs of segmentation are visible in future postotic somites at an early neurula stage, whereas the rostral mesoderm is unsegmented and rostromedially confluent with the prechordal plate. The premandibular and mandibular mesoderm develop from the prechordal plate in a caudal to rostral direction and can be called the preaxial mesoderm as opposed to the caudally developing gastral mesoderm. With the exception of the premandibular mesoderm, the head mesodermal sheet is secondarily regionalized by the otocyst and pharyngeal pouches into the mandibular mesoderm, hyoid mesoderm, and somite 0. The head mesodermal components never develop into cephalic myotomes, but the latter develop only from postotic somites. These results show that the lamprey embryo shows a typical vertebrate phylotype and that the basic mesodermal configuration of vertebrates already existed prior to the split of agnatha-gnathostomata; lamprey does not represent an intermediate state between amphioxus and gnathostomes. Unlike interpretations of theories of head segmentation that the mesodermal segments are primarily equivalent along the axis, there is no evidence in vertebrate embryos for the presence of preotic myotomes. We conclude that mesomere-based theories of head metamerism are inappropriate and that the formulated vertebrate head should possess the distinction between primarily unsegmented head mesoderm which includes preaxial components at least in part and somites in the trunk which are shared in all the known vertebrate embryos as the vertebrate phylotype.

Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits

“…A segmented vertebrate head upheld the argument for evolution by simple elaboration of the anterior part of an amphioxus-like ancestral animal. However, the bulk of morphological comparative data among different vertebrate species (29), as well as the absence of any periodical pseudosegmental structures in lampreys (30) and of comparable expression patterns of genes known to function in somitogenesis, present major obstacles to this hypothesis and instead support the absence of cephalic somitomeres in vertebrates.…”

The differentiation and morphogenesis of craniofacial muscles

“…The dorsomedial layer surrounding each head cavity forms a myotome-like epithelium that becomes associated with an EOM-innervating cranial nerve (III, oculomotor; IV, trochlear; and VI, abducens). Comparable head cavities/somites have since been described in several fish species (reviewed by Neal and Rand, 1940;Jarvik, 1980;Gilland and Baker, 1993), in Xenopus (Chung et al, 1989) but not other amphibians (Kuratani et al, 1999), and in Chelydra (snapping turtle, Johnson, 1913). Gilbert (1947Gilbert ( , 1957 identified mesenchymal condensations in early (25-30 somites) cat and human embryos that included primordia of extraocular muscles and within which small epithelial clusters formed (Gilbert, 1952).…”

“…These muscles historically were thought of as having evolved from an iterative set of serially homologous gill muscles, which together with gill skeletal elements constituted the branchiomeric apparatus (reviewed by Neal, 1918;Kuratani et al, 1999). Indeed, the branchial musculoskeletal system has often been touted as a novel and defining feature of vertebrates (reviewed in Gans and Northcutt, 1983;Hall, 2005;Northcutt, 2005).…”

Radiological trace of mandibular primary growth center in postnatal human mandibles

“…Particularly the mandible is associated with three different origins of muscle groups, i.e., masseter muscles originated from the first branchial arch, facial expression muscles originated from the second branchial arch, and lingual muscles originated from the occipital myotome (Lee et al, 1996;Kuratani et al, 1999). Therefore, the development of mandible shows heterogeneous morphology, which has been a major debating topic (Maddox et al, 1998;Ishizeki et al, 1999;Tavakkoli-Jou et al, 1999;Mina, 2001aMina, , 2001bWang et al, 2001).…”