Development of Cephalic Neural Crest Cells in Embryos of Lampetra japonica, with Special Reference to the Evolution of the Jaw

Abstract

Neural crest cells contribute extensively to vertebrate head morphogenesis and their origin is an important question to address in understanding the evolution of the craniate head. The distribution pattern of cephalic crest cells was examined in embryos of one of the living agnathan vertebrates, Lampetra japonica. The initial appearance of putative crest cells was observed on the dorsal aspect of the neural rod at stage 20.5 and ventral expansion of these cells was first seen at the level of rostral somites. As in gnathostomes, cephalic crest cells migrate beneath the surface ectoderm and form three major cell populations, each being separated at the levels of rhombomeres (r) 3 and r5. The neural crest seems initially to be produced at all neuraxial levels except for the rostral-most area, and cephalic crest cells are secondarily excluded from levels r3 and r5. Such a pattern of crest cell distribution prefigures the morphology of the cranial nerve anlage. The second or middle crest cell population passes medial to the otocyst, implying that the otocyst does not serve as a barrier to separate the crest cell populations. The three cephalic crest cell populations fill the pharyngeal arch ventrally, covering the pharyngeal mesoderm laterally with the rostral-most population covering the premandibular region and mandibular arch. The third cell population is equivalent to the circumpharyngeal crest cells in the chick, and its influx into the pharyngeal region precedes the formation of postotic pharyngeal arches. Focal injection of DiI revealed the existence of an anteroposterior organization in the neural crest at the neurular stage, destined for each pharyngeal region. The crest cells derived from the posterior midbrain that express the LjOtxA gene, the Otx2 cognate, were shown to migrate into the mandibular arch, a pattern which is identical to gnathostome embryos. It was concluded that the head region of the lamprey embryo shares a common set of morphological characters with gnathostome embryos and that the morphological deviation of the mandibular arch between the gnathostomes and the lamprey is not based on the early embryonic patterning.

Craniofacial development in marsupial mammals: Developmental origins of evolutionary change

“…Commonly in vertebrates, neural crest cells emerge after the neural folds have closed (e.g., Tosney, 1982;Hall and Horstadius, 1988;Epperlein and Löfberg, 1993;Hanken et al, 1997;Hall, 1999;Horigome et al, 1999;LeDouarin and Kalcheim, 1999;Falck et al, 2000), although in placental mammals and other vertebrates such as some anurans, neural crest emigration is initiated during neural fold elevation stages. In mice and rats, in which crest migration has been well studied, neural crest cells are generated at the future first arch region at the threesomite stage and first arch crest leaves the neural tube at approximately four to five somites, as the neural tube is beginning to close (Nichols, 1981(Nichols, , 1987.…”

Developmental Morphology of Branchiomeric Nerves in a Cat Shark, Scyliorhinus torazame, with Special Reference to Rhombomeres, Cephalic Mesoderm, and Distribution Patterns of Cephalic Crest Cells

“…Although SEM-based modern observations, like those by Horigome et al (1999), cannot conclude the absence of head cavities in cyclostome embryos (Horder et al, 2010), other histological observations failed to identify any head cavities, or mesodermal cysts in the cyclostome head mesoderm Oisi et al, 2013;Suzuki et al, 2016;Adachi and Kuratani, unpublished data): we propose that head cavities are most likely a gnathostome synapomorphy rather than an ancestral trait for all the vertebrates (as to the distribution of head cavities across vertebrates, see Gilbert, 1952).…”

Dissecting early regulatory relationships in the lamprey neural crest gene network

“…The basal-most extant vertebrates, lamprey and hagfish, are both agnathans (jawless vertebrates) that have migrating neural crest cells and most of the neural crest derivatives (7,(17)(18)(19)(20). Only lampreys reliably produce embryos that are accessible to experimental manipulation in the laboratory.…”