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)

Abstract

Background Despite the diverse morphology of the adult squamate naso-palatal complex – consisting of the nasal cavity, vomeronasal organ (VNO), choanal groove, lacrimal duct and superficial palate – little is known about the embryology of these structures. Moreover, there are no comprehensive studies concerning development of the nasal cavity and VNO in relation to the superficial palate. In this investigation, we used X-ray microtomography and histological sections to describe embryonic development of the naso-palatal complex of iguanian lizard, the brown anole (Anolis sagrei). The purpose of the study was to describe the mechanism of formation of adult morphology in this species, which combines the peculiar anole features with typical iguanian conditions. Considering the uncertain phylogenetic position of the Iguania within Squamata, embryological data and future comparative studies may shed new light on the evolution of this large squamate clade. Results Development of the naso-palatal complex was divided into three phases: early, middle and late. In the early developmental phase, the vomeronasal pit originates from medial outpocketing of the nasal pit, when the facial prominences are weakly developed. In the middle developmental phase, the following events can be noted: the formation of the frontonasal mass, separation of the vestibulum, appearance of the lacrimal duct, and formation of the choanal groove, which leads to separation of the VNO from the nasal cavity. In late development, the nasal cavity and the VNO attain their adult morphology. The lacrimal duct establishes an extensive connection with the choanal groove, which eventually becomes largely separated from the oral cavity. Conclusions Unlike in other tetrapods, the primordium of the lacrimal duct in the brown anole develops largely beyond the nasolacrimal groove. In contrast to previous studies on squamates, the maxillary prominence is found to participate in the initial fusion with the frontonasal mass. Moreover, formation of the choanal groove occurs due to the fusion of the vomerine cushion to the subconchal fold, rather than to the choanal fold. The loss or significant reduction of the lateral nasal concha is secondary. Some features of anole adult morphology, such as the closure of the choanal groove, may constitute adaptations to vomeronasal chemoreception.

Embryology of the naso‐palatal complex in Gekkota based on detailed 3D analysis in Lepidodactylus lugubris and Eublepharis macularius

“…The VNO duct opens on the palate and provides a direct connection between the VNO and the oral cavity. The separation of the VNO from the nasal cavity is associated with the formation of the choanal groove, which represents the ventral remnant of the embryonic nasal cavity (Bellairs & Boyd, 1950; Kaczmarek et al ., 2020). The choanal groove may provide the only indirect connection between the VNO duct and the nasal cavity or may be obliterated completely in some squamates (Malan, 1945; Gabe & Saint Girons, 1976).…”

“…The choanal groove may provide the only indirect connection between the VNO duct and the nasal cavity or may be obliterated completely in some squamates (Malan, 1945; Gabe & Saint Girons, 1976). More often it is retained in adults and forms a connection with the lacrimal duct (Bellairs & Boyd, 1950; Kaczmarek et al ., 2020).…”

“…The nasal cavity of squamates exhibits relatively simple morphology (Figure 1 and see introduction in Kaczmarek et al ., 2020). It consists of the tubular vestibulum, main nasal cavity, and outer choanal tube, which may form the nasopharyngeal duct in some taxa (Parsons, 1970).…”

“…The lateral nasal concha protrudes into the lumen of the main nasal cavity and divides it into the three parts which have different relations to the concha. These are the extraconchal space (lateral and dorsolateral), Stammteil (medial), and inner choanal tube (ventral and ventrolateral) (Fuchs, 1908; Parsons, 1959a, 1970; Kaczmarek et al ., 2020) (Figure 1).…”

“…Based on their ontogenetic and functional associations, the VNO, nasal cavity, lacrimal duct, choanal groove, and associated parts of the superficial (soft tissue) palate are called the naso‐palatal complex (Kaczmarek et al ., 2020).…”