Cranial osteogenesis in Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae)

Abstract

The pattern of onset and general rate of cranial ossification are compared in two marsupials, Monodelphis domestica (Didelphidae) and Macropus eugenii (Macropodidae). In both species a similar suite of bones is present at birth, specifically those surrounding the oral cavity and the exoccipital, and in both postnatal events follow a similar course. The facial skeleton matures more rapidly than the neurocranium, which is characterized by an extended period of ossification. Most dermal bones begin ossification before most endochondral bones. Endochondral bones of the neurocranium are particularly extended in both the period of onset of ossification and the rate of ossification. These data confirm suggestions that morphology at birth is conservative in marsupials and we hypothesize that the pattern of cranial osteogenesis is related to two distinct demands. Bones that are accelerated in marsupials are correlated with a number of functional adaptations including head movements during migration, attachment to the teat, and suckling. However, the very slow osteogenesis of the neurocranium is probably correlated with the very extended period of neurogenesis. Marsupials appear to be derived relative to both monotreme and placental mammals in the precocious ossification of the bones surrounding the oral cavity, but share with monotremes an extended period of neurocranial osteogenesis.

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.…”

“…Clark and Smith (1993) studied ossification sequence and pattern in Monodelphis domestica and Macropus eugenii. Cranial ossification patterns were also studied by Nesslinger (1956) and Frigo and Woolly (1996) in other marsupial species and confirm that the basic patterns presented by Clark and Smith for Monodelphis and Macropus are general patterns for marsupials.…”

“…Cranial ossification patterns were also studied by Nesslinger (1956) and Frigo and Woolly (1996) in other marsupial species and confirm that the basic patterns presented by Clark and Smith for Monodelphis and Macropus are general patterns for marsupials. Clark and Smith (1993) showed that the craniofacial skeleton ossified as two distinct units. The bones of the face are the first bones to begin ossification and also the first to complete ossification, whereas those of the neurocranium lag, with the exception of the exoccipital bone (which ossifies early as it serves as the attachment point of cervical muscles).…”

“…1991; Maier, 1993;Clark and Smith, 1993). Smith (1994) studied the development of craniofacial musculature in Monodelphis and compared it with patterns reported for eutherians.…”

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

“…Similar to the lamprey, marsupials are also critical to our understanding of heterochrony in neural crest cell development (Clark and Smith, 1993). Although marsupial mammals are born in a highly atricial state, the neonate must be capable of considerable functional independence.…”