Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Abstract

BackgroundSnakes are considered to be vomerolfaction specialists. They are members of one of the most diverse groups of vertebrates, Squamata. The vomeronasal organ and the associated structures (such as the lacrimal duct, choanal groove, lamina transversalis anterior and cupola Jacobsoni) of adult lizards and snakes have received much anatomical, histological, physiological and behavioural attention. However, only limited embryological investigation into these structures, constrained to some anatomical or cellular studies and brief surveys, has been carried out thus far. The purpose of this study was, first, to examine the embryonic development of the vomeronasal organ and the associated structures in the grass snake (Natrix natrix), using three-dimensional reconstructions based on histological studies, and, second, to compare the obtained results with those presented in known publications on other snakes and lizards.ResultsFive major developmental processes were taken into consideration in this study: separation of the vomeronasal organ from the nasal cavity and its specialization, development of the mushroom body, formation of the lacrimal duct, development of the cupola Jacobsoni and its relation to the vomeronasal nerve, and specialization of the sensory epithelium. Our visualizations showed the VNO in relation to the nasal cavity, choanal groove, lacrimal duct and cupola Jacobsoni at different embryonic stages. We confirmed that the choanal groove disappears gradually, which indicates that this structure is absent in adult grass snakes. On our histological sections, we observed a gradual growth in the height of the columns of the vomeronasal sensory epithelium and widening of the spaces between them.ConclusionsThe main ophidian taxa (Scolecophidia, Henophidia and Caenophidia), just like other squamate clades, seem to be evolutionarily conservative at some levels with respect to the VNO and associated structures morphology. Thus, it was possible to homologize certain embryonic levels of the anatomical and histological complexity, observed in the grass snake, with adult conditions of certain groups of Squamata. This may reflect evolutionary shift in Squamata from visually oriented predators to vomerolfaction specialists. Our descriptions offer material useful for future comparative studies of Squamata, both at their anatomical and histological levels.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-017-0188-y) contains supplementary material, which is available to authorized users.

Development of pancreatic acini in embryos of the grass snake Natrix natrix (Lepidosauria, Serpentes)

“…Eggs of the grass snake were incubated in a plastic hopper with a mixture of peat and sand at 30°C. Under these conditions, incubation lasted 30–33 days from oviposition to hatching (Hermyt, Kaczmarek, Kowalska, & Rupik, ; Kaczmarek, Hermyt, & Rupik, ; Rupik, , ). Embryos were sampled at regular intervals beginning from the time of egg laying.…”

Histomorphology of Vomeronasal Organ in Scincella tsinlingensis

“…The VNO of snakes and lizards, except for chameleons, was well developed and contained the SE of dorsal dome and NSE lined the ventral concha, which was called the mushroom body (Kaczmarek et al, 2017). The movement mechanism of chemicals through the vomeronasal fenestrae and into the lumen of VNO was related to the mushroom body.…”

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)

“…Despite the absence of the choanal groove -in most snakes [6,36,40] it has been shown to occur in the grass snake embryo (and probably in embryos of other snakes) and extends from the VNO duct to the outer choana [19]. Thus it is reasonable to assume that also in non-ophidian autarchoglossans, in which the choanal groove does not reach the VNO duct [36], the anterior part of the choanal groove becomes obliterated during a separate process.…”

“…It is worth noting that the nasopharyngeal duct of snakes and some lizards is not homologous with the nasopharyngeal duct of mammals and crocodiles [21,94]. The ophidian nasopharyngeal ducts of both sides join together in their posterior course and enter the oral cavity into the median palatal trough (orbitonasal trough) [6,17,19,21]. In this case the inner and outer choana become widely separated [6].…”