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.
Highlights
Amniotes (Amniota) consist of two large groups of tetrapod vertebrates, Synapsida and Reptilia, that diverged from one another over 300 million years ago (Ma) (Carroll, 1988, Modesto & Anderson, 2004, Benton, 2005)
We used a probe to Runx2, which is a molecular marker for osteogenic mesenchymal precursor cells (Ducy et al, 1997, Bobola et al, 2003, Abzhanov et al, 2007, Han et al, 2007, Kerney et al, 2010) and described its expression pattern in the temporal region of reptilian embryos where mineralization of bones has not been initiated
Differential expression of early osteoblast marker, Runx2, in the head of crocodile and turtle embryos Osteogenic mesenchymal precursor cells that express Runx2 are first detected in the temporal region of crocodile embryos at stage 14 (Additional file 1) and an almost identical pattern of Runx2 expression was observed in a subsequent embryonic stage
Summary
Amniotes (Amniota) consist of two large groups of tetrapod vertebrates, Synapsida and Reptilia, that diverged from one another over 300 million years ago (Ma) (Carroll, 1988, Modesto & Anderson, 2004, Benton, 2005). The lower temporal fenestra is dorsally surrounded by both the postorbital and squamosal bones, and ventrally by both the jugal and quadratojugal bones These temporal fenestrae are thought to have evolved to allow space for accommodating the enlarged jaw-closing muscles that enable powerful biting, or to minimize stresses exerted by the contraction of jaw muscles on the skull, or to reduce the weight of the skull itself (Frazzetta, 1968, Carroll, 1982, Rieppel, 1993a, Benton, 2005). Because the lower temporal bar that encloses the lower temporal fenestra ventrally is regarded to be lost once in the common ancestor of lepidosaurs (lizards, snakes, tuatara) and archosaurs (crocodiles and birds) (Rieppel, 1993a, Müller, 2003), these reptilian lineages possibly acquired the lower temporal bar secondarily (Müller, 2003, Moazen et al, 2009) Both snakes and birds have lost the upper temporal bar so that their temporal region is free from any bony frames (Pough et al, 2005)
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