The development of the osteocranium in the snake Psammophis sibilans (Serpentes: Lamprophiidae)

Abstract

Non‐avian reptiles are good models to investigate structural and developmental differences between amniotes. Investigations of craniofacial development in a complete series of embryos from oviposition up to hatching are still relatively rare. Consideration of a complete series can reveal developmental events that were previously missed, and thus correct or confirm theories about developmental events. The Egyptian Sand snake, Psammophis sibilans, has been a key species in descriptions of the snake skull development. However, published work was based on a limited sample of specimens collected from the wild. Here, we supplement previous descriptions with an illustrated account of skull development in P. sibilans based on a staged series of embryos and histological sections. Our findings largely agree with those of previous authors, although we record differences in developmental timing, confirming the presence of an egg tooth in this species. We add further observations on the enigmatic fenestra X, showing that it closes rather than merging with the prootic notch. Our observations revealed the likely contribution of the tectum posterius to the occipital roof, the presence of an internal carotid foramen (possibly transitory or variable), and the formation of the initial laterosphenoid pillar.

Insights into skull evolution in fossorial snakes, as revealed by the cranial morphology of Atractaspis irregularis (Serpentes: Colubroidea)

“…Heterochrony has been proposed as one of the major forces driving the evolution of the ophidian skull from that of nonophidian lizards (Da Silva et al , 2018; Hanken and Wake, 1993; Irish, 1989; Werneburg and Sánchez‐Villagra, 2015). Studies of snake skull ontogeny are still relatively rare, tending to focus on embryonic development (e.g., Pringle, 1954; Zehr, 1962; Jackson, 2002; Boughner et al , 2007; Boback et al , 2012; Polachowski and Werneburg, 2013; Khannoon and Evans, 2015; Khannoon and Zahradnicek, 2017; Sheverdyukova, 2017, 2019; Al‐Mohammadi et al , 2020; Khannoon et al , 2020), with only a few studies examining postnatal development (Young, 1989; Scanferla and Bhullar, 2014; Palci et al , 2016; Scanferla, 2016; Sherratt et al , 2019; Strong et al , 2019). However, our growing understanding of snake evolutionary development suggests that heterochrony is an important driver of the evolution not only of snakes relative to other squamates, but of snakes relative to each other (see also Da Silva et al , 2018).…”

Embryonic skull development in the gecko,Tarentola annularis(Squamata: Gekkota: Phyllodactylidae)

“…Psammophis , Al Mohammadi et al . 2019). However, in T. annularis , the opening seems to be the space between the prefacial and anterior basicapsular commissures that carries the facial nerve.…”

Embryonic development of skull bones in the Sahara horned viper (Cerastes cerastes), with new insights into structures related to the basicranium and braincase roof

“…However, at stage 30, corresponding to less than a quarter of the total post-ovipositional period (8 dpo), more than half of the bones analyzed such as premaxilla, maxilla, prefrontal, supratemporal, palatine, pterygoid, ectopterygoid, septomaxilla, dentary and compound bone have already started to ossify in Cerastes cerastes (Table 1). By contrast, the ossification pattern of the above mentioned bones is more gradual in Psammophis sibilans, starting first in supratemporal, palatine and compound bone (Table 2, rank 1), then in pterygoid, premaxilla, maxilla, prefrontal, ectopterygoid and dentary (ranks 2 and 3), and finally in septomaxilla (rank 5; Al Mohammadi et al, 2019). In Naja haje, ossification of these bones also starts at different developmental stages (Table 2; Khannoon and Evans, 2015), occurring more gradually than in Cerastes cerastes.…”

“…For this purpose, embryonic studies are absolutely needed to describe the timing of morphogenesis and ossification of individual skull bones in a specific taxon, which can be then directly used for the comparison of developmental events across species. So far, despite the numerous anatomical descriptions of adult skull bones in many different snake species (see review; Cundall and Irish, 2008), investigations of craniofacial development and morphology in complete snake embryonic series, from oviposition to hatching, are still relatively rare (Boughner et al, 2007;Boback et al, 2012;Polachowsky and Werneburg, 2013;Khannoon and Evans, 2015;Sheverdyukova, 2017;Al Mohammadi et al, 2019;Sheverdyukova, 2019). Major challenges in previous studies have been the difficulty in getting a representative panel of snake samples covering the complete embryonic period of skull development (Bellairs and Kamal, 1981;Kamal and Hammouda, 1965a;Kamal and Hammouda, 1965b) and the dependence on histological stainings of serial head sections for description (Hofstadler-Deiques, 2002;Hofstadler-Deiques et al, 2005).…”

“…For example, controversies exist regarding the laterosphenoid bone, particularly in the relative size of its dorsal and ventral components but also its formation by intramembranous ossification (Bellairs and Kamal, 1981). Similarly, the origin of the supraoccipital bone is highly debated, including in very recent studies (Khannoon and Evan, 2015;Al Mohammadi et al, 2019).…”