Development and evolution of the tetrapod skull–neck boundary

Abstract

The origin and evolution of the vertebrate skull have been topics of intense study for more than two centuries. Whereas early theories of skull origin, such as the influential vertebral theory, have been largely refuted with respect to the anterior (pre-otic) region of the skull, the posterior (post-otic) region is known to be derived from the anteriormost paraxial segments, i.e. the somites. Here we review the morphology and development of the occiput in both living and extinct tetrapods, taking into account revised knowledge of skull development by augmenting historical accounts with recent data. When occipital composition is evaluated relative to its position along the neural axis, and specifically to the hypoglossal nerve complex, much of the apparent interspecific variation in the location of the skull-neck boundary stabilizes in a phylogenetically informative way. Based on this criterion, three distinct conditions are identified in (i) frogs, (ii) salamanders and caecilians, and (iii) amniotes. The position of the posteriormost occipital segment relative to the hypoglossal nerve is key to understanding the evolution of the posterior limit of the skull. By using cranial foramina as osteological proxies of the hypoglossal nerve, a survey of fossil taxa reveals the amniote condition to be present at the base of Tetrapoda. This result challenges traditional theories of cranial evolution, which posit translocation of the occiput to a more posterior location in amniotes relative to lissamphibians (frogs, salamanders, caecilians), and instead supports the largely overlooked hypothesis that the reduced occiput in lissamphibians is secondarily derived. Recent advances in our understanding of the genetic basis of axial patterning and its regulation in amniotes support the hypothesis that the lissamphibian occipital form may have arisen as the product of a homeotic shift in segment fate from an amniote-like condition.

The broad role of Nkx3.2 in the development of the zebrafish axial skeleton

“…In gnathostomes, the most anterior somites contribute to the occipital bones [ 67 – 69 ]. The sclerotome from these occipital somites contributes to the basioccipital and exoccipital [ 70 – 72 ], so the occipital phenotypes observed in zebrafish and mouse Nkx3 .…”

The Broad Role of Nkx3.2 in the Development of the Zebrafish Axial Skeleton

“…In gnathostomes, the most anterior somites contribute to the occipital bones (Ferguson and Graham, 2004;Maddin et al, 2020;Morin-Kensicki et al, 2002). The sclerotome from these occipital somites contributes to the basioccipital and exoccipital (Couly et al, 1993;O'Rahilly, 2003, 1994), so the occipital phenotypes observed in zebrafish and mouse nkx3.2/Nkx3.2 mutants are consistent with the role of Nkx3.2 in the sclerotome.…”

Development and Evolution of the Skull-Neck Boundary: Insights from Amphibian Model Species

“…The number of somites that are incorporated into the occiput of the skull has been the subject of study for a long time up until today (e.g., Platt, 1897;Hunter, 1935;de Beer, 1937;Couly et al, 1993;Burke et al, 1995;Kuratani et al, 1999;Handrigan and Wassersug, 2007;Kuratani and Ota, 2008;Maddin et al, 2020). Early research using traditional techniques of histology and whole-mount embryology showed that agnathans (the jawless fishes) do not incorporate any somites into the head (Kuratani et al, 1999), whereas gnathostomes (jawed fishes plus tetrapods) do, and recruit a variable number of somites to form the bones of the occiput (de Beer, 1937).…”

“…One potential osteological correlate has been proposed for such investigations: foramina pertaining to the posterior-most cranial nerve, cranial nerve twelve (n.XII; Maddin et al, 2020), which is also generally referred to as the hypoglossal nerve or hypoglossal nerve complex in amniotes (de Beer, 1937;Romer and Edinger, 1942;Romer and Parsons, 1977;Grande and Bemis, 1998). As the most posteriorly situated cranial nerve, the hypoglossal nerve marks the boundary between cranial and spinal nerves (Barnard, 1940;Noden, 1983;Couly et al, 1993;Ferguson and Graham, 2004;Yaryhin and Werneburg, 2018).…”

“…These morphologies have not been confirmed in Xenopus laevis nor in Ambystoma mexicanum. Schematic synthesis based on Wake and Lawson (1973); Stuesse et al (1983); Hüppi et al (2019); Maddin et al (2020).…”