Skull Sutures and Cranial Mechanics in the Permian Reptile Captorhinus aguti and the Evolution of the Temporal Region in Early Amniotes

Abstract

While most early limbed vertebrates possessed a fully-roofed dermatocranium in their temporal skull region, temporal fenestrae and excavations evolved independently at least twice in the earliest amniotes, with several different variations in shape and position of the openings. Yet, the specific drivers behind this evolution have been only barely understood. It has been mostly explained by adaptations of the feeding apparatus as a response to new functional demands in the terrestrial realm, including a rearrangement of the jaw musculature as well as changes in strain distribution. Temporal fenestrae have been retained in most extant amniotes but have also been lost again, notably in turtles. However, even turtles do not represent an optimal analog for the condition in the ancestral amniote, highlighting the necessity to examine Paleozoic fossil material. Here, we describe in detail the sutures in the dermatocranium of the Permian reptile Captorhinus aguti (Amniota, Captorhinidae) to illustrate bone integrity in an early non-fenestrated amniote skull. We reconstruct the jaw adductor musculature and discuss its relation to intracranial articulations and bone flexibility within the temporal region. Lastly, we examine whether the reconstructed cranial mechanics in C. aguti could be treated as a model for the ancestor of fenestrated amniotes. We show that C. aguti likely exhibited a reduced loading in the areas at the intersection of jugal, squamosal, and postorbital, as well as at the contact between parietal and postorbital. We argue that these “weak” areas are prone for the development of temporal openings and may be treated as the possible precursors for infratemporal and supratemporal fenestrae in early amniotes. These findings provide a good basis for future studies on other non-fenestrated taxa close to the amniote base, for example diadectomorphs or other non-diapsid reptiles.

Evolution of the temporal skull openings in land vertebrates: A hypothetical framework on the basis of biomechanics

“…In this context, dorsal compression and ventral tension stresses in the skull might have been present, leaving the otic notch (i.e., suprafossal condition; Figures 15b and 18b) in the temporal region, which is typical for early tetrapods (Fröbisch & Witzmann, 2019). A spatial correspondence of the otic notch and the upper temporal opening has been demonstrated before (Abel et al, 2022a(Abel et al, , 2022bAbel & Werneburg, 2021;Kemp, 1982;Werneburg & Abel, 2022). Panchen (1964, p. 304) noted that "[the anatomy of the otic notch] gives support to Parrington's [Parrington, 1959] contention that the characteristic 'labyrinthodont' and 'cotylosaur' position of the otic notch are merely the result of differential growth of the cheek region, rather than migration of the tympanum from the former [posterior] position to the latter [more anterior one].…”

“…The regions at which these modules (i.e., functionally associated bones) meet each other are associated with those areas of the skull, in which, through amniote evolution, temporal openings may appear. By studying suture anatomy and thickness, Abel et al (2022a, 2022b) found further support for this conclusion. The authors have shown that these areas are less sutured and thinner in the skull of C. aguti .…”

“…One opening is also seen in many Permian parareptiles, which belong to the second major clade within Amniota, the Reptilia (as defined by Modesto and Anderson, 2004). Ancestrally, early Reptilia still preserve the anapsid skull condition (Abel et al, 2022a). One group, the reptilian Diapsida clade, however, shows a distinct supratemporal fenestra (Evans, 2008)-and some forms also have an infratemporal fenestra (together as "diplapsidy" sensu Werneburg, 2019).…”

“…Most likely, it is plesiomorphic for many early Reptilia, incl. Captorhinidae (Figure 8f*), but also for the earliest-most tetrapodomorphs such as Ichthyostega (Figure 18a) (Abel et al, 2022a(Abel et al, , 2022bAbel & Werneburg, 2024;Werneburg & Abel, 2022). We assume that tension and compression stresses were relatively low in all those animals (low magnitudes of anterior [M bpA ] and posterior perpendicular bite [M bpP ]; Figure 15a**) because no differentiation of the temporal region occurred and the fish-like, scutal condition of the skull was preserved (Figure 18a).…”

“…Some scutal taxa have very minute temporal openings along these unstressed areas (Abel & Werneburg, 2021). Those areas consist of little sutured bones (Abel et al, 2022a, 2022b) located at the intersection of different functional modules (Werneburg & Abel, 2022) of the skull. Three areas were identified (see Figure 8f*): (1) postorbital, parietal, and squamosum, (2) postorbital, squamosum, and jugal, and (3) jugal, quadratojugal, and squamosum.…”