Cranial neural crest cell migration in the Australian lungfish, Neoceratodus forsteri

Abstract

A crucial role for the cranial neural crest in head development has been established for both actinopterygian fishes and tetrapods. It has been claimed, however, that the neural crest is unimportant for head development in the Australian lungfish (Neoceratodus forsteri), a member of the group (Dipnoi) which is commonly considered to be the living sister group of the tetrapods. In the present study, we used scanning electron microscopy to study cranial neural crest development in the Australian lungfish. Our results, contrary to those of Kemp, show that cranial neural crest cells do emerge and migrate in the Australian lungfish in the same way as in other vertebrates, forming mandibular, hyoid, and branchial streams. The major difference is in the timing of the onset of cranial neural crest migration. It is delayed in the Australian lungfish in comparison with their living sister group the Lissamphibia. Furthermore, the delay in timing between the emergence of the hyoid and branchial crest streams is very long, indicating a steeper anterior-posterior gradient than in amphibians. We are now extending our work on lungfish head development to include experimental studies (ablation of selected streams of neural crest cells) and fate mapping (using fluoresent tracer dyes such as Dil) to document the normal fate as well as the role in head patterning of the cranial neural crest in the Australian lungfish.

Prosencephalic neural folds give rise to neural crest cells in the Australian lungfish, Neoceratodus forsteri

“…These include differentiation of cell precursors that form sensory placodal epithelium, as well as NC cells that infiltrate the frontonasal region of the lungfish head, and likely contribute to placodal precursors of the terminal nerve. These NC cells were not found in the Falck et al (2000) SEM study, so this study has extended the cranial NC of lungfish further rostrally than previously thought. Because lungfish are basal sarcopterygians, the lack of a premandibular NC stream in other anamniote tetrapods (amphibians) must now be questioned.…”

“…These cells must be the equivalent of the premandibular NC stream, previously only identified in amniote vertebrates. In further substantiation of this tentative conclusion, we have gone on to show that the unilateral ablation of discrete regions of the PNF, either dorsal or lateral to it, at a stage previously shown by Falck et al (2000) to be the commencement of cephalic NC migration (stage 24), produced unilateral effects on the development of the eye and olfactory organ.…”

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.…”

Morphogenesis of parrot jaw muscles: Understanding the development of an evolutionary novelty

“…The patterning of the cranial muscles is severely affected by the adjacent connective tissueforming mesenchyme, implying that the mesenchyme imparts spatial information upon the adjacent cranial muscle precursors through cell-cell interactions (Hall, 1950;Noden, 1986;Schilling et al, 1996;Schilling and Kimmel, 1997;Olsson et al, 2001). Therefore, modifications in the regulation of the neural crest cells are likely to have played a critical role in the generation of morphological diversity during vertebrate head evolution (Graveson, 1993;Bronner-Fraser, 1995;Hall, 1999;Falck et al, 2000;Smith, 2001;Schneider and Helms, 2003).…”