Abstract

Bones of the cranial vault appear to be highly conserved among tetrapod vertebrates. Moreover, bones identified with the same name are assumed to be evolutionarily homologous. However, recent developmental studies reveal a key difference in the embryonic origin of cranial vault bones between representatives of two amniote lineages, mammals and birds, thereby challenging this view. In the mouse, the frontal is derived from cranial neural crest (CNC) but the parietal is derived from mesoderm, placing the CNC–mesoderm boundary at the suture between these bones. In the chicken, this boundary is located within the frontal. This difference and related data have led several recent authors to suggest that bones of the avian cranial vault are misidentified and should be renamed. To elucidate this apparent conflict, we fate-mapped CNC and mesoderm in axolotl to reveal the contributions of these two embryonic cell populations to the cranial vault in a urodele amphibian. The CNC–mesoderm boundary in axolotl is located between the frontal and parietal bones, as in the mouse but unlike the chicken. If, however, the avian frontal is regarded instead as a fused frontal and parietal (i.e. frontoparietal) and the parietal as a postparietal, then the cranial vault of birds becomes developmentally and topologically congruent with those of urodeles and mammals. This alternative hypothesis of cranial vault homology is also phylogenetically consistent with data from the tetrapod fossil record, where frontal, parietal and postparietal bones are present in stem lineages of all extant taxa, including birds. It further implies that a postparietal may be present in most non-avian archosaurs, but fused to the parietal or supraoccipital as in many extant mammals.

Highlights

  • The cranial vault forms the roof of the vertebrate skull

  • We documented the contributions of both cranial neural crest (CNC) and cranial mesoderm to individual skull bones in the axolotl by transplanting green fluorescent protein (GFP)-labelled donor cells into wild-type hosts

  • It is generally assumed that the embryonic origin of the skull is highly conserved among tetrapods [17]

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Summary

Introduction

The cranial vault comprises numerous irregularly arranged bony plates, but during the evolution of tetrapods the number of separate bones is reduced and those that remain become organized into a regular and consistent pattern [1,2]. In primitive tetrapods, such as Acanthostega, the cranial vault consists of a longitudinal series of paired bones. Discrete postparietals are not seen in the adult skull of any living amphibian They are regarded as lost in all three extant groups, or alternatively that they are fused to the parietals in some or all species [10,11]. Living members of these lineages are widely considered to have lost postparietals, seemingly independently [13], there are accounts of postparietals in some crocodylian embryos [1,14]

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