Early differentiation and migration of cranial neural crest in the opossum, Monodelphis domestica

Abstract

Marsupial mammals are born at a highly altricial state. Nonetheless, the neonate must be capable of considerable functional independence. Comparative studies have shown that in marsupials the morphogenesis of many structures critical to independent function are advanced relative to overall development. Many skeletal and muscular elements in the facial region show particular heterochrony. Because neural crest cells are crucial to forming and patterning much of the face, this study investigates whether the timing of cranial neural crest differentiation is also advanced. Histology and scanning electron microscopy of Monodelphis domestica embryos show that many aspects of cranial neural crest differentiation and migration are conserved in marsupials. For example, as in other vertebrates, cranial neural crest differentiates at the neural ectoderm/epidermal boundary and migrates as three major streams. However, when compared with other vertebrates, a number of timing differences exist. The onset of cranial neural crest migration is early relative to both neural tube development and somite formation in Monodelphis. First arch neural crest cell migration is particularly advanced and begins before any somites appear or regional differentiation exists in the neural tube. Our study provides the first published description of cranial neural crest differentiation and migration in marsupials and offers insight into how shifts in early developmental processes can lead to morphological change.

Craniofacial development in marsupial mammals: Developmental origins of evolutionary change

“…In particular, it has been observed that, in marsupials, the tongue and oral apparatus are quite advanced, that there is a massive chondrocranium, but limited cranial ossification, that the secondary palate appears to close relatively early, that differences in the rate and pattern of dental development exist, that the jaw joint undergoes a "recapitulatory" transformation postnatally, and that the brain is relatively underdeveloped at birth. Smith and colleagues in a series of studies have examined craniofacial development in marsupials (Clark and Smith, 1993;Smith, 1994Smith, , 1996Smith, , 1997Smith, , 2001aSmith, ,b, 2002Smith, , 2003Nunn and Smith, 1998;Vaglia and Smith, 2003;van Nievelt and Smith, 2005a,b). This work has alternated between detailed model-system approaches using Monodelphis domestica as a case study, usually in comparison with the well studied murid rodents, with broader phylogenetic surveys.…”

“…In Monodelphis, neural crest cells begin to leave the neural plate at the beginning of stage 22, approximately 10 days after mating (Smith, 2001a;Vaglia and Smith, 2003) and a few hours after primitive streak formation. The stage 22 embryo consists of little more than a broad, flat neural plate.…”

Comparative analysis of neural crest cell death, migration, and function during vertebrate embryogenesis

“…SEM analyses of neural crest cell migration in marsupials suggest that several timing differences exist when compared with other vertebrates (Vaglia and Smith, 2003). In particular, the onset of cranial neural crest cell migration in opossums is very early relative to neural tube and somite development when compared with mouse and chick.…”

“…At this stage, which is before the initiation of somitogenesis, the neural plate is broad, flat, and open; however, preotic (presumptive r2/3 boundary) and otic (presumptive r5/6 boundary) sulci are clearly distinguishable in the neural plate. First arch neural crest cell migration commences during stage 22 in the region immediately anterior to the preotic sulcus (Vaglia and Smith, 2003). By stage 24 (six-to eight-somite stage), a substantial mass of cells has accumulated in the anterior region of the embryo as neural crest cells begin to differentiate into the broad swellings of the first (mandibular) branchial arch.…”

“…Toward the end of stage 25 (12-13 somites), the first and second branchial arches are clearly distinguishable, particularly the mandibular arch which spans the majority of the area ventral to the midbrain and rhombomeres 1 and 2. Neural crest cells continue to migrate into the mandibular and hyoid arch regions and posterior to the otic vesicle neural crest cells begin to condense at the level of the presumptive third branchial arch (Vaglia and Smith, 2003). Branchial arch neural crest cells migrate as a broad diffuse sheet similar to lamprey and axolotl; however, relatively few neural crest cells are generated at the level of rhombomeres 3 and 5 similar to mouse and chick embryos.…”