Skeletal gene expression in the temporal region of the reptilian embryos: implications for the evolution of reptilian skull morphology

Abstract

Reptiles have achieved highly diverse morphological and physiological traits that allow them to exploit various ecological niches and resources. Morphology of the temporal region of the reptilian skull is highly diverse and historically it has been treated as an important character for classifying reptiles and has helped us understand the ecology and physiology of each species. However, the developmental mechanism that generates diversity of reptilian skull morphology is poorly understood. We reveal a potential developmental basis that generates morphological diversity in the temporal region of the reptilian skull by performing a comparative analysis of gene expression in the embryos of reptile species with different skull morphology. By investigating genes known to regulate early osteoblast development, we find dorsoventrally broadened unique expression of the early osteoblast marker, Runx2, in the temporal region of the head of turtle embryos that do not form temporal fenestrae. We also observe that Msx2 is also uniquely expressed in the mesenchymal cells distributed at the temporal region of the head of turtle embryos. Furthermore, through comparison of gene expression pattern in the embryos of turtle, crocodile, and snake species, we find a possible correlation between the spatial patterns of Runx2 and Msx2 expression in cranial mesenchymal cells and skull morphology of each reptilian lineage. Regulatory modifications of Runx2 and Msx2 expression in osteogenic mesenchymal precursor cells are likely involved in generating morphological diversity in the temporal region of the reptilian skull.Electronic supplementary materialThe online version of this article (doi:10.1186/2193-1801-2-336) contains supplementary material, which is available to authorized users.

Palaeoneurological clues to the evolution of defining mammalian soft tissue traits

“…In Msx2 mutant humans this sometimes results in the persistence of a large circular opening on the midline between both parietal bones, reminiscent of the parietal foramen in NMT 52 . The activity of Msx2 has been linked to a number of developmental processes associated with the differentiation and proliferation of osteogenic cells, such as the morphogenesis and growth of the limbs 53 54 . In the skull, its expression is complemented by that of several other genes (e.g.…”

Integrating developmental biology and the fossil record of reptiles

“…In turtles, which have anapsid skull (i.e. with no fenestrae) -during embryonic growth Runx2 and Msx2 genes are expressed in mesenchymal cells in the temporal region, what results in complete temporal roofing (Tokita et al, 2013). It is possible that in other reptiles with anapsid skulls, like armoured pareiasaurs or procolophonids (all extinct), such pattern was present.…”

A developmental staging system and musculoskeletal development sequence of the common musk turtle (Sternotherus odoratus)

“…Turtles are among the most transformed of all amniotes, bearing many unique features, most notably a rigid trunk encased in a carapace. Their peculiar anatomy has made them the object of several embryological studies focusing on the development and evolution of the turtle shell, [1][2][3][4][5][6][7][8][9] shoulder, [10][11][12] head, 13 skull, [14][15][16][17][18][19][20] and general skeletal development. [21][22][23][24][25][26][27][28][29][30][31] Developmental staging systems have been described for members of several clades of turtles (Figure 1), including.…”