Recent insights into the morphological diversity in the amniote primary and secondary palates

Abstract

The assembly of the upper jaw is a pivotal moment in the embryonic development of amniotes. The upper jaw forms from the fusion of the maxillary, medial nasal, and lateral nasal prominences, resulting in an intact upper lip/beak and nasal cavities; together called the primary palate. This process of fusion requires a balance of proper facial prominence shape and positioning to avoid craniofacial clefting, whilst still accommodating the vast phenotypic diversity of adult amniotes. As such, variation in craniofacial ontogeny is not tolerated beyond certain bounds. For clarity, we discuss primary palatogenesis of amniotes into in two categories, according to whether the nasal and oral cavities remain connected throughout ontogeny or not. The transient separation of these cavities occurs in mammals and crocodilians, while remaining connected in birds, turtles and squamates. In the latter group, the craniofacial prominences fuse around a persistent choanal groove that connects the nasal and oral cavities. Subsequently, all lineages except for turtles, develop a secondary palate that ultimately completely or partially separates oral and nasal cavities. Here, we review the shared, early developmental events and highlight the points at which development diverges in both primary and secondary palate formation.

Keywords: choana; craniofacial; lip fusion; palatal shelves; primary palate; reptile.

Figure 1

Digitally reconstructed optical projection tomography (OPT) scans of embryos depicting the medial nasal prominences, mnp (purple); lateral nasal prominence, lnp (red); maxillary prominence, mxp (green), and reptile frontonasal mass, fnm (purple). A) E11.5 mouse (Mus musculus); B) 10-day crocodile (Crocodilus niloticus(Peterka et al., 2010); C) stage 28 chicken (Gallus gallus - (Hamburger and Hamilton, 1951); D) stage 4 turtle (Emydura subglobosa - (Werneburg et al., 2009); E) stage 34 chameleon (Chamaeleo calyptratus(Blanc, 1974). A’) High magnification of mouse fusion zone depicting the lambdoid (λ) junction as white dashed lines at the boundary where all three prominences meet. Figure modified from (Abramyan et al., 2015).

Figure 2

Illustration depicting the two mechanisms of craniofacial prominences unification. A) Fusion is depicted in posterior frontal section of E11.5 mouse embryo, between the maxillary and the medial nasal prominences. Fusion is illustrated as a three stage process: stage i, prominences attach and a bilayered epithelial seam forms between the tissues; stage ii, the bilayered epithelial seam begins to break down through apoptosis, cell migration, or epithelialmesenchymal transformation; stage iii, the mesenchyme between the two prominences unifies into a single structure with shared mesenchyme and tissues fill in. B) Merging is depicted in the same embryo as occurring in the nasolacrimal groove, which demarcates the boundary between the lateral nasal and maxillary prominences. During merging, the superficial groove fills in and becomes a smooth surface on the embryo. Figure modified from our previous work (Abramyan et al., 2015).

Figure 3

Illustrations of histological sections of E11.5 mouse embryo in the frontal plane. A) Anterior-most section illustrates fusion between the medial nasal and lateral nasal prominences. B) Posterior sections, on the other hand, show fusion as occurring between the medial nasal and maxillary prominences. The exact position of the prominences is demarcated by the nasolacrimal groove (black arrowhead). The site of bucconasal membrane formation at the site of fusion is also between the maxillary and medial nasal prominences (red arrowhead). Epithelial tissue in the nasal cavity and brain are depicted in grey. br, brain; lnp, lateral nasal prominence; mnp, medial nasal prominences; mxp, maxillary prominence; md, mandible; nc, nasal cavity; nf, nasal fin.

Figure 4

Schematic summarizing the two modes of primary palate fusion. Steps a - c depict processes in primary palate fusion that are conserved in all amniotes, although the actual prominences which initiate the fusion varies according to taxon. Steps d and e depict Fusion Modes 1 and 2 respectively. In step d, just posterior to the mesenchymal bridge unifying the primary palate, the epithelial seam (nasal fin) persists, forming a transient bucconasal membrane. In e, there is no epithelial seam posterior to the primary palate; instead entering the choanal groove. In the transverse plane (α), the decline in proliferation at the base of the choana (lighter grey) allows for the groove to remain as the prominences grow around it. The final state (f) in all amniotes is in an open choana connecting the oral and nasal cavities. bn, bucconasal membrane; cg, choanal groove. Figure modified from (Abramyan et al., 2015).

Figure 5

External views of amniote palates at late fetal stages. The secondary palate in the mouse and alligator is completely closed (A,B). In the chicken, there is a cleft between the palatal shelves, but the shelves still cover most of the palate (C). The chameleon also exhibits relatively substantial palatal shelves (D). In the leopard gecko, the palatal shelves are highly reduced (demarcated by white, dashed lines) (E). This gives access to the vomeronasal organ, located in the roof of the mouth. In the turtle, there are no palatal shelves, and the choanae (internal nares) open directly into the oral cavity (F). c, choana; ps, palatal shelf; pv, palatal valve; sp, secondary palate. Scale bars: 2mm (A,B,C,E,F); 1mm (D)

Figure 6

Illustrations depicting palatal views of the three lineages with secondary, bony palates which have independently evolved in amniotes. A) The canine skull represents the mammalian lineage. The mammalian secondary palate involves only three bones, the premaxilla, maxilla and the palatine. B) The crocodilian phenotype is represented by the American alligator (Alligator mississippiensis). In the crocodilian secondary palate, the secondary palate involves substantial input from the pterygoids, which also envelop the choanae entirely. C) The sea turtle is represented by the olive ridley turtle (Lepidochelys olivacea) (illustrated from (Wyneken and Witherington, 2001). In the sea turtle, the secondary palate has substantial input from the vomer, which is not observed in either mammals or crocodilians. pmx, premaxilla; psph, presphenoid; sq, squamosal; bsph, basisphenoid; ecpt, ectopterygoid; pt, pterygoid; q, quadrate; max, maxilla; pal, palatine; j, jugal; vom, vomer.