Novel insights into the development of the avian nasal cavity

Abstract

In embryonic amniotes, patterning of the oral and nasal cavities requires bilateral fusion between craniofacial prominences, ensuring an intact primary palate and upper jaw. After fusion has taken place, the embryonic nasal cavities open anteriorly through paired external nares positioned directly above the fusion zones and bordered by the medial nasal and lateral nasal prominences. In this study, we show that in the chicken embryo, the external nares initially form as patent openings but only remain so for a short period of time. Soon after the nasal cavities form, the medial nasal and lateral nasal prominences fuse together in stage 29 embryos, entirely closing off the external nares for a substantial portion of embryonic and fetal development. The epithelium between the fused prominences is then retained and eventually develops into a nasal plug that obstructs the nasal vestibule through the majority of the fetal period. At stage 40, the nasal plug begins to break down through a combination of cellular remodeling, apoptosis, as well as non‐apoptotic necrosis, leading to completely patent nasal cavities at hatching. These findings place chickens in a category with several species of nonavian reptiles and mammals (including humans) that have been found to develop a transient embryonic nasal plug. Our findings are discussed in the context of previously reported cases of nasal plugs as part of normal embryonic development and provide novel insight into the craniofacial development of a key model organism in developmental biology.

Development of the squamate naso-palatal complex: detailed 3D analysis of the vomeronasal organ and nasal cavity in the brown anole Anolis sagrei (Squamata: Iguania)

“…In fact, at the time of separation of the external naris and the primitive outer choana, which occurs at stage 8 of the brown anole (Movie S1), the external naris and the vestibulum are sealed by the well developed nasal plug. Similar "delay" in formation of the nasal plug, which has been noted in turtle, may occur in birds (see [71]). These facts may explain the description of Abramyan et al [67], who did not nd the closed external naris in turtle and chick in stages at the time of initial fusion of facial prominences.…”

“…As he stated, the amniotic uid may still reaches the lumen of the main nasal cavity through the open choana (see also [67]). Moreover, despite the fact that recanalization of the vestibulum takes place shortly before hatching in the brown anole (this study) and in other extant sauropsids [72], in some mammals including human, the reduction of the nasal plug occurs relatively early [71,72,76].…”

“…The presence of the embryonic nasal plug is a common transient embryonic feature of amniotes. It has been found in snakes [66,69,72], lizards [18,73], turtle [69], Sphenodon [74], birds [71,72] and mammals [72,75] including human [76,77]. The nature of the nasal plug is poorly understood.…”

“…It is described as mass of epithelial cells [75], mass of isodiametric cells [21], peridermal plug [72,78], or structure formed by keratinocytes [77]. It has been proposed that it forms between the nasal prominences from the epithelial seam, which does not undergo disintegration [71,72], or as a proliferation of the "invaginated" oral epithelium [78], which in fact may be considered as walls of the presumptive vestibulum. It seems to us that these explanations are not mutually exclusive.…”

“…3B and S2A) resembles a multilayered medial edge epithelial seam in the human embryonic soft palate (see [79]), although in the anole the basal layer, which forms the walls of the future vestibulum, can easily be distinguished. Distribution of the nasal plug is restricted to the vestibulum in later embryonic life [21,71,72].…”