Osteogenic gene expression in the temporal region of the opossum embryos: an insight into the evolution of synapsid skull unique to mammalian lineage.

Abstract

The skull of amniotes is categorized into three conditions based on skeletal arrangement in the temporal region: anapsid, synapsid and diapsid. Mammals (class Mammalia), a descendent lineage of the clade Synapsida, possess the synapsid skull, which is characterized by a single lower temporal arch that ventrally borders the lower temporal fenestra. Although we previously suggested, based on the data from placental mammals, that the reduction in the expression domain of the upstream osteogenic genes Msx2 and Runx2 in the embryonic temporal mesenchyme might have played a role in the evolution of synapsid skulls, the molecular basis of synapsid skull evolution is still largely unknown. In this study, we investigated expression patterns of four osteogenic genes (two upstream genes Msx2 and Runx2 and two downstream genes Sp7 and Sparc) in the embryonic and neonatal temporal region of the gray short-tailed opossum Monodelphis domestica, the most commonly used experimental marsupial model, in order to more thoroughly understand the molecular basis of development of synapsid skulls unique to mammals. We found that M. domestica embryos and neonates display very restricted expressions of Msx2 and/or Runx2 in the dermal bone precursors in the temporal region, as two placental species do (the house mouse Mus musculus and the greater horseshoe bat Rhinolophus ferrumequinum). Spatially restricted expression of Msx2 and Runx2 in the embryonic temporal region may be a foundation for creating the "advanced" synapsid skull shared by all mammals where only three dermal bones configure the temporal region.