Resolving homology in the face of shifting germ layer origins: Lessons from a major skull vault boundary

Abstract

The vertebrate skull varies widely in shape, accommodating diverse strategies of feeding and predation. The braincase is composed of several flat bones that meet at flexible joints called sutures. Nearly all vertebrates have a prominent 'coronal' suture that separates the front and back of the skull. This suture can develop entirely within mesoderm-derived tissue, neural crest-derived tissue, or at the boundary of the two. Recent paleontological findings and genetic insights in non-mammalian model organisms serve to revise fundamental knowledge on the development and evolution of this suture. Growing evidence supports a decoupling of the germ layer origins of the mesenchyme that forms the calvarial bones from inductive signaling that establishes discrete bone centers. Changes in these relationships facilitate skull evolution and may create susceptibility to disease. These concepts provide a general framework for approaching issues of homology in cases where germ layer origins have shifted during evolution.

Keywords: developmental biology; evolutionary biology; homology; skull; sutures.

Figure 1.. Schematics and nomenclature of major skull vault bones and sutures.

(A) Diagrams of normal and synostotic human skulls. Bones are labeled in black and sutures in blue. Asterisks denote the missing coronal suture in Saethre-Chotzen Syndrome skulls. (B) Major skull vault bones and sutures in dorsal views (anterior to the left). Current names are listed on top, and suggested names for zebrafish are listed at bottom. Note that in the revised naming of zebrafish bones, the zebrafish coronal suture is analogous to the lambdoid suture of mouse as the murine interparietal is a fusion of postparietals and tabulars.

Figure 2.. Evolution of the coronal suture and associated skull bones.

Skull bones associated to the ‘coronal suture’ are mapped on a phylogeny of selected extant and extinct osteichthyans. On one side of each skull, bones are color-coded based on deductions from evolutionary continuity – for example the actinopterygian ‘parietal’ is what was formerly referred to as the ‘frontal’ in these species. The pineal foramen is shown by a black dot. The currently accepted coronal suture is shown for Danio (zebrafish), Mus (mouse), and Columba (pigeon). Daggers denote extinct species represented only by fossils.

Figure 3.. Neural crest-mesoderm boundaries relative to the coronal suture.

Schematics depict neural crest (teal) and mesoderm (yellow) contributions to skull bones of lineage-traced model organisms. Red line indicates the position of the suture commonly referred to as the ‘coronal suture’ in each respective species, though this may not be reflective of a true coronal suture.

Figure 4.. Models of brain to skull interactions across vertebrates.

(A) Cranial bones are depicted relative to embryonic brain, with crest-derived bone in teal and mesoderm-derived bone in yellow. Comparison of zebrafish, chick, and mouse proposes the zona limitans intrathalamica (ZLI) and midbrain-hindbrain boundary (MHB, or isthmic organizer) as major signaling centers for suture development. For chick, two interpretations are shown: ‘chick A’ in which the mesoderm-derived portion of the ‘frontal’ bone is homologous to the anterior part of the mammalian parietal, and ‘chick B’ in which the mesoderm-derived postorbital is fused to the frontal. (B) Signaling molecules enriched at the ZLI and MHB include Wnts, Fgfs, En1/2, and Shh, all of which have known roles in proper skull and suture formation. F, frontal; P, parietal; IP, interparietal; SO, supraoccipital; PO, postorbital; tel, telencephalon; di, diencephalon; mid, midbrain; hind, hindbrain; ZLI, zona limitans intrathalamica; MHB, midbrain-hindbrain boundary; cor, coronal suture; lam, lambdoid suture; OP, occipitointerparietal suture.