Two braincases of Daspletosaurus (Theropoda: Tyrannosauridae): anatomy and comparison1
Abstract
For sheer complexity, braincases are generally considered anatomically conservative. However, recent research on the braincases of tyrannosaurids have revealed extensive morphological variations. This line of inquiry has its root in Dale Russell’s review of tyrannosaurids in which he established Daspletosaurus torosus — a large tyrannosaurine from the Campanian of southern Alberta. In the wake of systematic revisions to tyrannosaurines previously assigned to Daspletosaurus, one potentially distinct species remains undescribed. This paper describes and compares a braincase referable to this species with that of the holotype for Daspletosaurus torosus using computerized-tomography-based reconstructions. The two braincases have numerous differences externally and internally. The specimen of Daspletosaurus sp. has a bottlenecked olfactory tract, short and vertical lagena, and a developed ascending column of the anterior tympanic recess. The holotype of Daspletosaurus torosus has many unusual traits, including an anteriorly positioned trochlear root, elongate common carotid canal, distinct chamber of the basisphenoid recess, asymmetry in the internal basipterygoid aperture, and laterally reduced but medially expanded subcondylar recess. This comparison also identified characters that potentially unite the two species of Daspletosaurus, including deep midbrain flexures in the endocasts. However, many character variations in the braincases are known in other tyrannosaurids to correlate with body size and maturity, or represent individual variations. Therefore, taxonomic and phylogenetic signals can be isolated from background variations in a more comprehensive approach by using additional specimens. New information on the two braincases of Daspletosaurus is consistent with the emerging view of tyrannosaurid braincases as highly variable, ontogenetically dynamic character complexes.
Résumé
Du seul point de vue de la complexité, l’anatomie des boîtes crâniennes est généralement considérée comme étant conservative. Des recherches récentes sur les boîtes crâniennes de tyrannosauridés ont toutefois révélé une grande variabilité morphologique. Cette avenue d’étude prend sa source dans la synthèse sur les tyrannosauridés de Dale Russell, dans laquelle l’auteur établit Daspletosaurus torosus, un grand tyrannosauriné du Campanien du sud de l’Alberta. À la suite de révisions systématiques de tyrannosaurinés précédemment affectés à Daspletosaurus, une espèce potentiellement distincte demeure non décrite. Le présent article décrit une boîte crânienne pouvant être référée à cette espèce et la compare à celle de l’holotype de Daspletosaurus torosus en utilisant des reconstitutions basées sur la tomographie par ordinateur. De nombreuses différences tant externes qu’internes existent entre les deux boîtes crâniennes. Le spécimen de Daspletosaurus sp. présente des voies olfactives en goulot d’étranglement, une lagéna courte et verticale, ainsi qu’une colonne ascendante développée du récessus tympanique antérieur. L’holotype de Daspletosaurus torosus présente de nombreux caractères inhabituels, dont une racine trochléaire positionnée antérieurement, un canal carotidien commun allongé, une cavité distincte du récessus basisphénoïde, une asymétrie de l’ouverture basiptérygoïde interne et un récessus subcondylaire réduit latéralement, mais agrandi médialement. Cette comparaison fait également ressortir des caractères qui pourraient unir les deux espèces de Daspletosaurus, dont de profondes flexures mésencéphales dans les endocastes. Il est toutefois établi que de nombreuses variations de caractères dans les boîtes crâniennes chez d’autres tyrannosauridés sont corrélées à la taille du corps et à la maturité ou représentent des variations individuelles. Des signaux taxonomiques et phylogénétiques peuvent donc être isolés des variations de fond par une approche plus exhaustive en faisant appel à d’autres spécimens. Les nouveaux renseignements sur les deux boîtes crâniennes de Daspletosaurus concordent avec l’opinion émergente selon laquelle les boîtes crâniennes de tyrannosauridés constituent des complexes de caractères très variables et dynamiques sur le plan ontogénique. [Traduit par la Rédaction]
Introduction
The description of Daspletosaurus torosus Russell, 1970 ushered in the modern era of research on North American tyrannosaurids. To Dale A. Russell, erecting Daspletosaurus was not a simple taxonomic act, but was the result of his synthesis of anatomy, palaeoecology, and taxonomy of the tyrannosaurids known at that time from the Late Cretaceous of North America (Russell 1970). This led him to envisioning multiple genera of large, anatomically distinct carnivorous dinosaurs coexisting on a Campanian coastal floodplain by partitioning their niches: Daspletosaurus as a more robust form specialized in feeding on ceratopsians, and Gorgosaurus (regarded by him as a synonym of Albertosaurus) as a more gracile form with a preference for hadrosaurs (Russell 1970).
On the eve of the 21st century, as Russell completed his work on Canadian dinosaurs and moved to North Carolina, Daspletosaurus remained as the more elusive taxon among the tyrannosaurid genera known from the Campanian and Maastrichtian of western North America (Laramidia). Conventionally, non-albertosaurine tyrannosaurids from the Campanian strata of Laramidia were then referred to as Daspletosaurus sp. in the absence of taxonomic alternatives (Carpenter 1992; Carr 1999; Holtz 2001, 2004; Currie 2003a, 2003b). As a result, the literature available at the time suggested that the genus Daspletosaurus had unusually broad distribution for a large theropod: the Kirtland Formation of New Mexico, the Two Medicine Formation of Montana, and the Oldman and Dinosaur Park formations of Alberta. Now, the Kirtland taxon is recognized as its own genus and species, Bistahieversor sealeyi (Carr and Williamson 2000, 2010). The Two Medicine form is designated as a distinct species, Daspletosaurus horneri (Horner et al. 1992; Currie et al. 2005; Carr et al. 2017). Although undescribed at the time, the subsequent decades brought two more genera of Campanian tyrannosaurines from Utah: Lythronax argestes (Wahweap Formation) (Loewen et al. 2013) and Teratophoneus curriei (Kaiparowits Formation) (Carr et al. 2011; Loewen et al. 2013). Additionally, Nanuqsaurus hoglundi is a tyrannosaurine from the Maastrichtian Prince Creek Formation of Alaska (Fiorillo and Tykoski 2014). Possibly the most recent member on this list, tyrannosaurid material collected from the Foremost Formation of Alberta has been proposed as a distinct taxon, Thanatotheristes degrootorum (Voris et al. 2020). Characters of the frontal used to diagnose this taxon have been critically reviewed (Yun 2020).
Despite this rapid increase in taxonomic understanding, Daspletosaurus — the “prototypical” Campanian tyrannosaurine — stands on thin literature. The original description (Russell 1970) established the taxonomy and provided an anatomical summary of the holotype CMN 8506 (Oldman Formation, Alberta) with several reconstructions (skeletal mount; skull in lateral and dorsal views; palate in ventral view), measurements, and two photographic plates of the forelimb. Of the specimens assigned to Daspletosaurus torosus by Russell (1970), AMNH 5438 (paratype), CMN 350, and UALVP 11 are each represented by a partial postcranial skeleton and are neither diagnostic (Currie 2003b) nor relevant to the present study. This leaves AMNH 5346, CMN 11594, and NHMUK R4863 (all from the Dinosaur Park Formation) as eligible for comparison with the holotype. In the extensive revision of the cranial anatomy of tyrannosaurids from Alberta, Currie (2003a) considered these specimens as anatomically distinct from Daspletosaurus torosus. His description is based on these and new specimens of Daspletosaurus discovered from either the Dinosaur Park Formation or the chronologically equivalent upper levels of the Oldman Formation (FMNH PR308, TMP 85.62.1, TMP 92.36.1220, TMP 94.143.1, TMP 2001.36.1). The idea that Daspletosaurus from the Dinosaur Park Formation is distinguished from Daspletosaurus torosus at species level has been presented preliminarily in the literature (Bakker et al. 1988; Currie 2003a, 2005; Loewen et al. 2013). Currently, the descriptive work for this species is ongoing by the second and last authors of this paper, primarily focused on TMP 2001.36.1.
Some specimens referred to as Daspletosaurus are controversial. Russell (1970) included CMN 11315 — a partial skull and skeleton of a tyrannosaurid from the Horseshoe Canyon Formation of Alberta (Maastrichtian) — as possibly representing a distinct species within Daspletosaurus. CMN 11315 is now considered likely to represent an immature individual of Albertosaurus (Mallon et al. 2020). FMNH PR308 was identified as Gorgosaurus (or Albertosaurus libratus at the time) by Russell (1970), but later revised as Daspletosaurus (Carr 1999; Currie 2003a). An isolated frontal from the Dinosaur Park Formation (SDNHM 32701) was assigned to Daspletosaurus torosus (Yun 2020), but suites of characters present in this specimen only suggest tyrannosaurine affinity. Yun (2020) assigned SDNHM 32701 to Daspletosaurus based on the longitudinal ridge on the nasal process. Although sometimes used as an autapomorphy of Daspletosaurus (Carr et al. 2017), this character is a correlate of the frontal–nasal suture, is influenced by body size, and has a broader distribution. Furthermore, the communication with T.D. Carr cited by Yun (2020) to suggest the holotype of Daspletosaurus torosus (CMN 8506) as collected from the Dinosaur Park Formation is erroneous, because the locality for CMN 8506 (Quarry 72) clearly sits below the Oldman – Dinosaur Park boundary (Currie 2005).
TMP 94.143.1 — a well-preserved skull and skeleton of an immature tyrannosaurid from the Dinosaur Park Formation — was originally described as Daspletosaurus (Currie 2003a), but recently proposed as Gorgosaurus (Voris et al. 2019). In this paper, TMP 94.143.1 continues to be treated as an immature individual of Daspletosaurus. The basis for Voris et al. (2019) to remove this specimen from Daspletosaurus both assumes and requires a single character in the postorbital (“cornual process”, the rugose mass of bone independent from the orbital margin) to be an ontogenetically constant diagnostic character of the taxon. The argument was formulated on finding this character expressed in an isolated postorbital (TMP 2013.18.11) slightly smaller than that of TMP 94.143.1, which lacks the cornual process. Voris et al. (2019) proceed to score allometrically variable characters in TMP 94.143.1 for a phylogenetic analysis, which found the specimen nested outside tyrannosaurines and with more gracile albertosaurines. This phylogenetic “slippage” appears consistent with a broadly observed artifact of confusing allometric and ontogenetic variations with taxonomically significant characters, which was predicted by controlled analyses of juvenile specimens (Campione et al. 2013).
Accepting this phylogenetic outcome, Voris et al. (2019) never ruled out alternative interpretations for observed character variations: the cornual process may be variably developed in Daspletosaurus among immature individuals, or the thickened orbital margin in TMP 2013.181.11 may represent an abnormal condition (which might call into a question the identification of TMP 2013.181.11 as Daspletosaurus). Other characters cited by Voris et al. (2019) as additional evidence for the Gorgosaurus affinity of TMP 94.143.1 are inconclusive. These characters are either pathologically modified in that specimen (maxillary tooth count) or variable within species (postorbital–squamosal contact is polymorphic in Gorgosaurus, Tarbosaurus, and Tyrannosaurus; shape of the ventral ramus of a postorbital correlates with body size). They also ignored a number of characters identified in TMP 94.143.1 by Currie (2003a) to indicate its affinity with Daspletosaurus (e.g., frontal–nasal suture; dorsal ramus of lacrimal; pneumatopore and form of orbital margin of jugal). This taxonomic note is important because in this paper TMP 94.143.1 represents a comparative specimen within Daspletosaurus. These taxonomic disagreements are due partly to the lack of robust diagnosis for species of Daspletosaurus and partly to the limited information in the literature about the anatomy of the genus.
In this paper, two well-preserved braincases of Daspletosaurus are three-dimensionally reconstructed based on computerized tomography (CT) scans and described. TMP 2001.36.1 (Daspletosaurus sp.) is a nearly complete skull and skeleton of an ontogenetically mature individual from the Oldman Formation in the southeastern corner of Alberta, Canada. Chronologically, the Oldman Formation in this region is equivalent to the upper part of the Dinosaur Park Formation (unpublished data; Federico Fanti, personal communication, 2021). CMN 8506 (Daspletosaurus torosus) is the holotype and is represented by a skull and skeleton of an ontogenetically mature individual, which comes from 100 km farther north from the Oldman Formation outcropping in Dinosaur Provincial Park. The quarry is overlain by the type section of the Dinosaur Park Formation. The braincases of both specimens were described cursorily and illustrated superficially in previous works, but this paper will provide details of the osteology, endocasts (including the inner ear), and pneumaticity. There will also be morphological comparisons with other tyrannosaurid braincases.
Institutional abbreviations
AMNH, American Museum of Natural History, New York, USA; CMN, Canadian Museum of Nature, Ottawa, Canada; CMNH, Cleveland Museum of Natural History, Cleveland, USA; FMNH, Field Museum of Natural History, Chicago, USA; ICM, the Children’s Museum of Indianapolis, Indianapolis, USA; IGM, Institute of Geology, Mongolian Academy of Sciences, Ulanbaatar, Mongolia (now merged with MPC-D); LACM, Los Angeles County Museum of Natural History, Los Angeles, USA; MCF-PVPH, Museo Carmen Funes, Plaza Huincul, Argentina; MOR, Museum of the Rockies, Bozeman, USA; MPC-D, Institute of Paleontology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia; NHMUK, Natural History Museum, London, United Kingdom; NMMNH, New Mexico Museum of Natural History, Albuquerque, USA; PIN, Paleontological Institute of the Russian Academy of Sciences, Moscow, Russia; ROM, Royal Ontario Museum, Toronto, Canada; RSM, Royal Saskatchewan Museum, Eastend, Canada; SDNHM, San Diego Natural History Museum, San Diego, USA; TMP, Royal Tyrrell Museum of Palaeontology, Drumheller, Canada; UMNH, Utah Museum of Natural History, Salt Lake City, USA; ZPAL, Institute of Palaeobiology of the Polish Academy of Sciences, Warsaw, Poland.
Materials and methods
CMN 8506 is the holotype of Daspletosaurus torosus from the Oldman Formation of Dinosaur Provincial Park, southern Alberta, and includes a complete braincase (Fig. 1). TMP 2001.36.1 belongs to an undescribed species of Daspletosaurus that occurs from chronologically younger strata than that for CMN 8506. The specimens referable to this undescribed species are known from the Dinosaur Park Formation and the chronologically equivalent part of the Oldman Formation (Currie 2003a). TMP 2001.36.1 was collected from the Milk River Natural Area, southern Alberta (precise locality information is available from TMP upon request). When collected, the braincase of TMP 2001.36.1 was separated into two parts (Fig. 2): skull roof (associated with the ethmoid complex, laterosphenoids, orbitosphenoids, and supraoccipital) and the basicranium (associated with the otoccipitals and prootics). These two complexes fit almost perfectly (Fig. 3).
Fig. 1.
Fig. 2.
Fig. 3.
CMN 8506 was CT scanned using a medical tomographer Toshiba Aquilion at the X-ray computed tomographic scanning facility of Montfort Hospital (Ottawa, Ontario), applying 135 kV and 300 mA, resulting in 1215 slices (pixel size = 0.976 mm). The two parts of the braincase of TMP 2001.36.1 were CT scanned separately. The skull roof was scanned using a medical tomographer General Electrics Light Speed at Canada Diagnostic Center (Calgary, Alberta), applying 140 kV and 227.21 mA, resulting in 469 slices (pixel size = 0.631 mm, slice increment = 1.249 mm). The rest of the braincase was scanned using a medical tomographer Siemens Sensation 64 at the University of Alberta Hospital (Edmonton, Alberta), applying 120 kV and 210 mA, resulting in 657 slices (pixel size = 0.941 mm, slice increment = 0.59 mm).
To reconstruct the braincase of CMN 8506 and its internal structures, 3D Slicer version 4.10.2 (Fedorov et al. 2012) was used to segment the bone, endocranial cavity, canals for nerves and major vessels, and pneumatic recesses. For reconstruction of the braincase of TMP 2001.36.1, Materialise Mimics version 18.0 (Materialise NV) was used. In the braincase of CMN 8506, internal space remains filled with cement-rich, fine-grained sandstone that possibly has high iron content. It is difficult to delineate the bone-matrix boundary, especially in small internal structures such as the canals for the abducens nerve. In principle, missing portions may be interpolated for up to 2 cm if the bone-matrix boundaries are clearly delineated at both ends. No structure was extrapolated. Several examples of the interpretations made to identify the boundary are provided in Supplementary Figs. S1 and S22. Anatomical terminology and colour codes for the CT-based rendering follow those of Witmer and Ridgely (2009).
Description
The braincases of CMN 8506 (Fig. 1) and TMP 2001.36.1 (Figs. 2 and 3) are well ossified (all the ethmoid elements are preserved as ossifications), but the sutures remain incompletely closed in both specimens. In TMP 2001.36.1, the skull roof and basicranial complexes meet in an open suture at the laterosphenoid–prootic contact. Although the braincase of CMN 8506 is intact, the same suture is clearly visible between the laterosphenoid and prootic. Most sutures remain unclosed in both braincases, except for the fused otoccipital (opisthotic + exoccipital), the single parietal, and the indiscernible basisphenoid–parasphenoid contact. This is consistent with other tyrannosaurid braincases, including those of ontogenetically mature tyrannosaurines (Bistahieversor: NMMNH P-37469; Lythronax: UMNH V 20200; Tarbosaurus: MPC-D 107/05; Tyrannosaurus: AMNH 5029, AMNH 5117, MOR 008, RSM P2523.8) (Osborn 1912; Carr and Williamson 2010; Loewen et al. 2013). The sutures separating the basioccipital, basisphenoid, laterosphenoid, otoccipital, and prootic from each other begin to close toward the size extreme (Tarbosaurus: ZPAL MgD-I/4; Tyrannosaurus: BHI 3033, MOR 555, MOR 1125) (Currie 2003a; Hurum and Sabath 2003), although these sutures curiously remain visible in one of the largest and most mature specimens of Tyrannosaurus (RSM P2523.8) (Persons et al. 2020). In Daspletosaurus, the sutures in the braincase are generally more closed in CMN 8506 than in TMP 2001.36.1 (Fig. 3). The basioccipital and otoccipital are separated by an externally open suture toward the base of the metotic strut in TMP 2001.36.1, whereas in CMN 8506 the same suture is recognized externally as a narrow line between the coalescing edges of the bones.
It is not clear whether these differences in braincase ossification indicate relatively mature status of CMN 8506 with respect to TMP 2001.36.1 or individual variations in the development of braincase sutures. In dinosaurs, a braincase tends to close the sutures at early ontogenetic stages (Currie 1997). Tyrannosaurines are an interesting exception, as most braincase elements are delineated by externally visible sutures in animals as large as AMNH 5117 and RSM P2523.8 (Tyrannosaurus), CMN 8506 (Daspletosaurus torosus) and TMP 2001.36.1 (Daspletosaurus sp). Such loosely ossified braincases may be rare but are not unique among theropods. In all the tyrannosaurid braincases, the exoccipital and opisthotic form a single element (termed here as otoccipital). However, the two bones are independent from one another in several theropod braincases, including those of Baryonyx, Coelophysis, and Gallimimus (Osmólska et al. 1972; Raath 1978; Colbert 1989; Charig and Milner 1997). The prootic–epiotic suture observed on the dorsal region of the vestibular eminence of TMP 2001.36.1 is also visible in Aucasaurus garridoi (MCF-PVPH 236) (Paulina-Carabajal and Succar 2014) (Fig. 4).
Fig. 4.
Frontal
Left and right frontals are clearly separated by a midline suture in both CMN 8506 and TMP 2001.36.1. The suture is a vertical, linear contact anteriorly and becomes progressively interdigitated posteriorly. This posterior interdigitate portion appears to have been extensively vascularized by the network of the supraorbital arteries and veins. A series of grooves connects the posterior interfrontal contact and the orbital notch, as they delineate the anterior margin of the supratemporal fossa. Near the medial ends of these grooves, a vascular foramen opens on the midline in CMN 8506, where the thickened interfrontal contact separates the left and right supratemporal fossae. In TMP 2001.36.1, this foramen opens on the right side, perforating the frontal. This vascular foramen may be unique to tyrannosaurines. It is present on the midline in other tyrannosaurine specimens (Daspletosaurus: CMN 11841; Tyrannosaurus: RSM P283), whereas it is absent in albertosaurines (Albertosaurus, TMP 81.10.1; Gorgosaurus, TMP 94.12.602). As in many large theropods, more than half of the dorsally exposed surfaces of the frontals are occupied by the supratemporal fossae. The anterolateral margin of the fossa meets the anterior extreme of the postorbital laterally. A shallow groove extends from the supraorbital notch (gap between the postorbital and lacrimal) and delineate the supratemporal fossa.
The frontals and co-ossified parietals (subsequently referred to as the parietal) meet to form a sagittal peak where the parietal wedges between the left and right frontals at the midline. The peak is continuous posteriorly with the sagittal crest of the parietal and anteriorly with the thickened interfrontal contact. Laterally, the frontal–parietal contact forms the anterior wall of the adductor chamber that sits within the supratemporal fenestra (Holliday and Witmer 2007; Holliday et al. 2020). The thickened suture allows the supratemporal fossa to expand posteriorly and hang slightly over the adductor chamber. This overhang is observed broadly among large theropods, including Aucasaurus (Paulina-Carabajal and Succar 2014), Gorgosaurus (TMP 94.12.602), Murusraptor (Coria and Currie 2016), and Sinraptor (Currie and Zhao 1993a).
Parietal
The frontals and parietal occupy semi-equal lengths of the skull roof. In dorsal view, the parietal has a more transversely oriented contact with the frontals in large tyrannosaurines than in albertosaurines, and relatively small individuals of tyrannosaurines (e.g., TMP 94.143.1). The interfrontal peak becomes tall enough to make the sagittal crest concave in each of the transverse profiles of CMN 8506 and TMP 2001.36.1, whereas the interfrontal peak is markedly lower than the nuchal crest in albertosaurines (Currie 2003a). CMN 8506 and TMP 2001.36.1 differ from each other in development of the sagittal crest. The crest is tall and thin with a knife-like edge in CMN 8506, whereas it is low and thick with a round dorsal edge in TMP 2001.36.1. Taxonomic significance of this difference remains to be determined. Some specimens of Daspletosaurus sp. from the Dinosaur Park Formation (TMP 85.62.1, TMP 94.143.1) each have a thin sagittal crest with sharp edge, whereas others (FMNH PR308) are intermediate between CMN 8506 and TMP 2001.36.1. The character may be taxonomically significant, but the polymorphism implies other correlates of variation — allometric, individual, or ontogenetic. In Daspletosaurus, the nuchal crest is comparatively low in profile with respect to mature individuals of Tarbosaurus and Tyrannosaurus: the supraoccipital forms more than half the height from foramen magnum to the top of the nuchal crest (at the midline) in both CMN 8506 and TMP 2001.36.1. A pair of concavities develops on the posterior surface of the nuchal crest, immediately above the supraoccipital knobs. The concavities are separated from each other by a thin vertical ridge. In TMP 2001.36.1, each of these concavities has a deep pit tucked behind the supraoccipital knobs. These are insertions of the muscle spinalis capitis, and are better developed in large tyrannosaurines than in albertosaurines (Snively and Russell 2007; Tsuihiji 2010).
Supraoccipital
The supraoccipital is relevant to this description in two respects. First, it is hollow (has a supraoccipital sinus). Second, it delimits the foramina for the posterior mid-cerebral veins. Both of these features are discussed in the following sections dealing with the renderings. In TMP 2001.36.1, the dorsal half of the supraoccipital is damaged, revealing the supraoccipital sinus (Figs. 2D and 2E). The suture between the supraoccipital and parietal is open internally. The open suture clearly shows contribution of the supraoccipital to the endocranial cavity.
Basioccipital
The basioccipital forms three quarters of the occipital condyle and extends anteriorly as a narrow midline strip between the otoccipitals from the foramen magnum to the neck of the condyle. Below the occipital condyle, the basioccipital contacts the basisphenoid anteriorly down to the basal tubera, and the otoccipital laterodorsally. Within the space defined by these contacts, the basioccipital also accommodates the paired subcondylar fossae, each with a pneumatopore beside the neck of the occipital condyle, immediately below the vagal and hypoglossal foramina. A marked difference between CMN 8506 and TMP 2001.36.1 is in the height of the basioccipital relative to the entire occiput. In CMN 8506, the basioccipital is so low that the occipital condyle and basal tubera are separated from each other vertically for the height of the condyle. In contrast, the basioccipital is taller in TMP 2001.36.1, with the occipital condyle-tuber distance being almost one and a half times the height of the condyle. This variation comes partly from the difference in dimensions of the occipital condyle relative to the occiput between the two specimens. However, the low basioccipital profile of CMN 8506 is similar to that seen in an albertosaurine, whereas the condition in TMP 2001.36.1 is consistent with tyrannosaurines in general (Currie 2003a). As discussed at the outset, the basioccipital sutures tend to be better ossified in CMN 8506 than in TMP 2001.36.1. In the latter specimen, the basioccipital forms an open suture with the otoccipital and basisphenoid (Figs. 2D, 2F, 3C, 3G). The suture with the otoccipital is closing on the occipital condyle but is still visible.
Basisphenoid and parasphenoid
As the largest single block in the basicranium, the basisphenoid and parasphenoid house four distinct pneumatic systems: the anterior tympanic, basipterygoid, basisphenoid, and subsellar recesses (Figs. 5 and 6) (Currie 2003a). In ventral view, the basisphenoid recess is defined by bony walls connecting the four corners, which are the paired basal tubera and basipterygoid processes (Bakker et al. 1988). The basipterygoid process extends more ventrally and laterally than the basal tuber, causing the basisphenoid recess to open posteroventrally (Currie 2003a). In both CMN 850 and TMP 2001.36.1, the extended ventral margin of the basisphenoid meets that of the paroccipital process at approximately 130° (CMN 8506: 135°; TMP 2001.36.1: 128°). The basal tubera are well developed in CMN 8506 with each having a distinct neck, whereas each basal tuber in TMP 2001.36.1 is only visible in lateral view as the corner defined by the ventral and posterior outlines of the basicranium. These two specimens differ from each other in other traits of the basicranial profile (e.g., relationship between the metotic strut and paroccipital process), but these features will be discussed in the section on the otoccipital.
Fig. 5.
Fig. 6.
The basisphenoid recess extends deeply toward the endocranial floor, which in CMN 8506 becomes paired concavities. Anterior to this main basisphenoid recess, the paired basipterygoid recesses pneumatize the interbasipterygoid lamina and basipterygoid processes. As in most tyrannosaurids (Bakker et al. 1988; Currie 2003a; Witmer and Ridgely 2009), the basipterygoid recesses communicate with the basisphenoid recess through paired diverticula in TMP 2001.36.1. However, CMN 8506 departs from this pattern in having the basipterygoid recesses largely distinct from the basisphenoid recess, and also having a well-developed anterodorsal median chamber derived from the basisphenoid recess. These characters are discussed in detail in the section dedicated to the pneumaticity.
The anterior tympanic recess has its pneumatopore tucked under the ala basisphenoidalis (the wing-like basisphenoidal portion of the preotic pendant) and is spatially associated with the internal carotid foramen (Witmer and Ridgely 2009). TMP 2001.36.1 has a prominent ala basisphenoidalis that curves toward the basal tuber with a rugose edge, whereas that in CMN 8506 extends straight ventrally toward the basipterygoid process. TMP 94.143.1 is similar to TMP 2001.36.1 in having a prominent, curved ala basisphenoidalis (Currie 2003a). As a site of attachment for the muscle protractor pterygoideus (Holliday 2009), the difference in the shape of the ala basisphenoidalis appears to be ontogenetically robust and may be taxonomically significant. The basipterygoid process is directly below the ala basisphenoidalis as in most tyrannosaurids. It is pneumatized at its base by the basipterygoid recess.
The parasphenoid is fused to the basisphenoid in both CMN 8506 and TMP 2001.36.1. The cultriform process is damaged in both specimens, revealing the acute triangular cross section of the subsellar recess. In TMP 2001.36.1, the hypophyseal fossa is visible because the laterosphenoid (attached to the skull roof complex) has separated from the rest of the braincase. The exposed hypophyseal fossa in TMP 2001.36.1 reveals the common carotid canal (a confluence between left and right internal carotid arteries) just below the laterosphenoid–basisphenoid contact. The lateral wall of the fossa is thin, only about 5 mm at the thickest.
Otoccipital (exoccipital + opisthotic)
Perhaps the most complex among braincase elements, the otoccipital partly houses the labyrinth (inner ear) and the largest pneumatic system in the braincase (posterior tympanic recess), transmits four distinct cranial nerves (CN IX–XII), and forms the following parts of the braincase: paroccipital process, metotic strut, lateral neurocranial wall, much of the foramen magnum, and small part of the occipital condyle (Figs. 5 and 6). As in other tyrannosaurid braincases, the crista tuberalis separates the glossopharyngeal (CN IX) and vagal (CN X+XI) foramina, representing the lateral edge of the metotic strut (a bony wall that forms from the metotic cartilage and separates the glossopharyngeal and vagal/jugular canals; sensu Witmer 1990; Currie and Zhao 1993b). The vagal foramen opens at the base of the neck for the occipital condyle, immediately ventral to the hypoglossal foramina (CN XII) and dorsal to the pneumatopore for the subcondylar recess (Fig. 3). In TMP 2001.36.1, the contact surface with the prootic is exposed on the anterior surface of the paroccipital process. This delineates the otosphenoidal crest — a posterior projection that overlaps the otoccipital at the base of the paroccipital process. The columellar groove extends below this contact. Posteriorly, a pneumatopore opens within the otoccipital, immediately dorsal to the columellar passage. This is one of the two major pneumatopores into the posterior tympanic recess (the other opens on the posterodorsal surface of the paroccipital process). Anteriorly, the columella extends the length of the paroccipital process, reaching the columellar recess (and the fenestra ovalis internally). A nearly complete columella (diameter = 2.3 mm) is preserved in situ on the right side of TMP 2001.36.1.
The main difference in the otoccipitals of CMN 8506 and TMP 2001.36.1 is in the development of the crista tuberalis. In CMN 8506, the ventral margin of the paroccipital process meets the crista tuberalis at a nearly perpendicular angle, forming a deep embayment at the base of the process (Figs. 1A and 1B). In contrast, the crista tuberalis is well-developed in TMP 2001.36.1 so that it extends from the ventral margin of the paroccipital process, forming a smooth transition ventrally in a gently concave outline in lateral view (Figs. 2 and 3).
Prootic
The prootic contacts the laterosphenoid anteriorly, and this suture remains open in TMP 2001.36.1 (Fig. 3). The prootic has a prominent otosphenoidal crest, the ventral margin of which (crista prootica) hangs over and delineates the columellar groove. It overlaps the otoccipital toward the base of the paroccipital process, whereas the lower portion of the prootic only extends as posterior as the fenestra ovalis (tucked inside the columellar recess). The columellar recess and the recess for the maxillomandibular (CN V2+3) and facial (CN VII) foramina are separated by a low bony ridge extending from the otosphenoidal crest. Referred to here as subotic process, the same structure is present in other tyrannosaurids, including an immature individual of Daspletosaurus (TMP 94.143.1) as well as other theropods including Allosaurus, Piatnitzkysaurus, and Sinraptor (Madsen 1976; Currie and Zhao 1993a; Rauhut 2004; Paulina-Carabajal and Currie 2012). Anteriorly across the maxillomandibular and facial foramina, the prootic extends as a downward bony process to overlap the ala basisphenoidalis laterally (here referred to collectively as a preotic pendant). In TMP 2001.36.1, an open suture separates this prootic portion of the preotic pendant from the ala basisphenoidalis. The contribution of the prootic to the preotic pendant extends as ventrally as the border of the pneumatopore for the anterior tympanic recess.
Set between the preotic pendant and subotic process, the facial and maxillomandibular foramina open in a small recess (Fig. 3). The maxillomandibular foramen is large and oval, whereas the facial foramen is smaller and sits immediately posterodorsal to the former. CMN 8506 and TMP 2001.36.1 are nearly identical in these morphological traits, but differ from each other in the otosphenoidal crest and maxillomandibular/facial recess. In TMP 2001.36.1, the otosphenoidal crest and subotic process are more pronounced and the preotic pendant recurves more strongly than in the other specimen. The otosphenoidal crest of CMN 8506 is not swollen laterally as it is in TMP 2001.36.1. Accordingly, the subotic process is nearly flat and not accompanied by the ventral bulge in the crista prootica. The preotic pendant is nearly straight in CMN 8506, which correlates with a difference in the shape of the ala basisphenoidalis.
Internally, the prootic forms a large portion of the otic capsule. The medial wall has a protuberance known as vestibular eminence. As observed in TMP 2001.36.1, a vertical suture extends on the eminence to separate the probable epiotic (which is indistinguishably fused to the supraoccipital) and prootic (Fig. 4). Although this suture is usually fused in theropods, it is present and visible in Aucasaurus (Paulina-Carabajal and Succar 2014) and probably in Tyrannosaurus (as shown by Witmer and Ridgely 2009; Fig. 7A). In TMP 2001.36.1, the floccular recess opens on the anterior surface of the vestibular eminence and has a figure-eight outline because of a constriction separating the vertical slit into smaller dorsal and larger ventral lobes. This condition occurs in Abelisaurus and Aucasaurus (Paulina-Carabajal and Succar 2014), although the recess is typically oval or subcircular in Tyrannosaurus (Witmer and Ridgely 2009) and other theropods, including Giganotosaurus, Murusraptor, Piatnitzkysaurus, Sinraptor, and Stenonychosaurus (Currie and Zhao 1993b; Coria and Currie 2002; Rauhut 2004; Paulina-Carabajal and Currie 2012, 2017).
Fig. 7.
Laterosphenoid
The laterosphenoid is the most anterior of all the braincase elements that are penetrated by the cranial nerves derived from the rhombencephalon. The laterosphenoid transmits the ophthalmic branch of the trigeminal nerve (CN V1), which enters the braincase at the base of the postorbital process. CN V1 extends within the intraosseous canal across the open prootic–laterosphenoid suture and enters the endocranial cavity through a separate internal foramen from that for the maxillomandibular nerve (Figs. 3D and 3E). This makes the nerve an interesting exception among the cranial nerves that otherwise penetrate a single bone or extend across a closed or fused contact. The laterosphenoid also transmits two of the three motor nerves that innervate the extraocular muscles (CN III and CN IV, oculomotor and trochlear nerves, respectively) and forms the posterior margin of the optic foramen (CN II).
Together with the basisphenoid and parasphenoid, the laterosphenoid is part of a major strut from the skull roof (frontal) to the palate (basipterygoid process), which forms the deepest vertical dimension of the braincase. Unlike facial elements, contacts between these bones are either fused or wide and interdigitated with the exception of the palatal contact (between the basipterygoid process and pterygoid). Therefore, development of the relatively tall profile of a mature tyrannosaurine skull correlates with the morphology of this strut. It curves posteriorly in albertosaurines and immature tyrannosaurines (e.g., TMP 94.143.1), whereas it is vertical in mature tyrannosaurines including CMN 8506 and TMP 2001.36.1. The functional importance of the laterosphenoid in both supporting the cranial vault and suspending the palate is ontogenetically consistent from its initial development as the pila antotica in a chondrocranium (De Beer 1937), and as seen later in forming a robust lateral wing (postorbital process) to secure broad contact area with the frontal and postorbital.
Orbitosphenoid and ethmoid complex
At the anterior end of the neurocranium, the orbitosphenoid and ethmoid complex are ossified in CMN 8506 and TMP 2001.36.1 as in other mature tyrannosaurids. The orbitosphenoid sits between the ethmoid complex and the laterosphenoid, and its posterior margin forms the anterior half of the optic foramen (CN II). Dorsally, the orbitosphenoid wedges between the laterosphenoid and sphenethmoid to contact the frontal for a short distance. This orbitosphenoid–frontal contact is a general condition among tyrannosaurids (including CMN 8506, TMP 94.143.1, and TMP 2001.36.1) (Osborn 1912; Brochu 2003; Ali et al. 2008; Bever et al. 2013). However, the orbitosphenoid appears to be excluded from the frontal by the laterosphenoid–sphenethmoid contact in CMN 11841, which is referred to as Daspletosaurus sp. (Currie 2003a). This laterosphenoid–sphenethmoid contact is possibly an overgrowth that covers the orbitosphenoid contribution to the frontal contact. However, this cannot be determined externally in this specimen.
The ethmoid complex has been interpreted variably. This paper follows the scheme by Ali et al. (2008) in which the midline septum represents a mesethmoid and the lateral trough on either side a sphenethmoid (Fig. 1E). These two bones are completely ossified in both CMN 8506 and TMP 2001.36.1. However, they are not preserved as bony elements in smaller individuals such as TMP 94.143.1. Based on the impressions on the ventral side of the frontal, these immature specimens likely had these elements as cartilages, yet to be ossified. United along the midventral suture, the left and right sphenethmoids form a U-shaped outline in anterior view to house the olfactory bulbs. In Gorgosaurus (e.g., TMP 94.12.602; ICM 2001.891), the left and right sphenethmoids meet each other mid-dorsally as well as mid-ventrally to assume an oval profile in anterior view. This latter condition is also observed in abelisaurids and carcharodontosaurids (Paulina-Carabajal and Currie 2012). The mesethmoid separates the left and right olfactory bulbs. Orientations of the olfactory nerves can be tracked along anteroposterior striations on the internal surfaces of the element.
Cranial endocast
Various attempts have been made to determine how closely a cranial endocast (infilling of the endocranial cavity) follows brain morphology (Osborn 1912; Hopson 1977, 1979, 1980; Brochu 2000; Morhardt 2016). Endocasts provide hard maxima for the soft tissues, but often inferences are lacking to estimate how much of any endocranial cavity a brain may have occupied. Vascular imprints on the endocranial wall are considered as an osteological correlate for thin meninges appressed against the bone. Among theropods, ornithomimids, oviraptorids, and troodontids are known to have on the skull roof such imprints of blood vessels of the dural envelope (Russell 1969, 1972; Currie 1985; Osmólska 2004). Similar vascular impressions are also known from tyrannosaurids, implying these animals had relatively large brains that mostly filled the endocranial cavities (Witmer and Ridgely 2009). The vascular imprints on the internal surface of the laterosphenoid of TMP 2001.36.1 (Fig. 7) support this interpretation. Interestingly, these vascular impressions occur primarily in frontals among small to mid-sized theropods (Russell 1969, 1972; Currie 1985; Osmólska 2004), including juveniles of Tarbosaurus (MPC-D107/10; MPC-D107/13). In mature tyrannosaurids, the vascular impressions are either faint or non-recognizable in the cerebral region, but the best examples occur in the lateral endocranial walls (Witmer and Ridgely 2009). These trends suggest changing relationships between the brain and endocranial cavity across age and size among tyrannosaurids.
The endocasts reconstructed for CMN 8506 and TMP 2001.36.1 (Figs. 8 and 9) are consistent with those for Tyrannosaurus in overall shapes and proportions except for two features — the dural peak (or dorsal expansion) and the midbrain flexure. In CMN 8506 and TMP 2001.36.1, the dural peak is not markedly higher than the cerebral hemisphere or the olfactory bulb. This is similar to the endocast for Tarbosaurus (Saveliev and Alifanov 2007) and one specimen of Tyrannosaurus (AMNH 5117) (Witmer and Ridgely 2009). However, the endocasts each have a markedly distinct, dorsally projecting dural peak in other specimens of Tyrannosaurus (AMNH 5029; CMNH 7541; FMNH PR2081) and at least one specimen each of Alioramus (MPC-D 100/1844) and Gorgosaurus (ROM 1247) (Osborn 1912; Brochu 2000; Witmer and Ridgely 2009, 2010; Bever et al. 2013). Variation among the mature specimens of Tyrannosaurus suggests that relative prominence of a dural peak may vary at the level of individuals rather than across age, size, or species. In comparison with the endocasts of Tyrannosaurus (Osborn 1912; Brochu 2000; Witmer and Ridgely 2009, 2010), those of CMN 8506 and TMP 2001.36.1 each have a strongly sigmoidal profile due to the pronounced midbrain flexure. This is similar to the endocast of one specimen of Gorgosaurus (ROM 1247) (Witmer and Ridgely 2009).
Fig. 8.
Fig. 9.
Forebrain
In both CMN 8506 and TMP 2001.36.1, the olfactory tract is clearly separated from the cerebral hemispheres by a transverse constriction. In TMP 2001.36.1, the tract is markedly narrow both vertically and transversely with respect to the cerebral region and olfactory bulbs, similar to the endocasts of Alioramus, Bistahieversor, and Gorgosaurus (Witmer and Ridgely 2010; Bever et al. 2013; McKeown et al. 2020). However, CMN 8506 is more consistent with other large tyrannosaurines in having an olfactory tract that is not so bottlenecked as in TMP 2001.36.1 (Osborn 1912; Brochu 2000; Witmer and Ridgely 2009; Bever et al. 2013). The cerebral hemispheres are weakly expanded laterally. In both CMN 8506 and TMP 2001.36.1, the optic fenestra is a single structure, and the left and right optic nerves are not clearly separated from each other in either endocast. This appears to be a general condition among large tyrannosaurines. The optic nerves enter the braincase through a single fenestra in mature specimens of Tyrannosaurus (Osborn 1912; Witmer and Ridgely 2009) but they clearly have a separate foramen on each side in CMNH 7541 (Witmer and Ridgely 2010) and at least one specimen each of Alioramus (MPC-D 100/1844) (Bever et al. 2013) and Daspletosaurus (TMP 94.143.1). The single optic fenestra of TMP 2001.36.1 is incipiently constricted at the midline (Fig. 3D), whereas the outline is smoothly oval in CMN 8506.
The hypophyseal fossa is intact in CMN 8506, but is damaged in TMP 2001.36.1. The hypophysis is vertical in CMN 8506, even though the descending structure tends to have a posteriorly curved profile in tyrannosaurids (Hopson 1979; Brochu 2000; Witmer and Ridgely 2010). The cerebral branch of the internal carotid artery enters the endocranial space at the bottom of the hypophyseal fossa. In CMN 8506, the common (= midline) carotid canal is unusually long and oriented more ventrally than posteriorly (Fig. 8). The latter feature (orientation of the carotid canal) as well as a straight hypophysis occurs in CMNH 7541 (Witmer and Ridgely 2009, 2010). Unlike CMNH 7541, however, the common carotid canal in CMN 8506 extends as posteriorly as the root of the ophthalmic branch of the trigeminal nerve (CN V1). At least one specimen of Gorgosaurus (ROM 1247) has this condition (Witmer and Ridgely 2009), but the canal extends at a much shallower angle than in CMN 8506 (angle of carotid canal against the long axis of the fore-midbrain in CMN 8506: 57°; AMNH 5117: 44°; AMNH 5029: 40°; CMNH 7541: 59°; ROM 1247: 29°).
Midbrain
No mesencephalic structure is apparent in either CMN 8506 or TMP 2001.36.1, and the optic lobe cannot be delineated precisely (Figs. 8, 9). This appears to be a general condition among tyrannosaurids (Witmer and Ridgely 2009). The oculomotor and trochlear nerves (CN III and CN IV) each have their independent roots on the ventral side, which Russell (1970) considered erroneously to have shared a single canal. The oculomotor canal has a larger diameter than the trochlear canal, but its reconstructed volume on the right side of CMN 8506 reflects contralateral variation of canal size and potentially represents an abnormal or pathological state (Figs. 1E, 8). On that side of CMN 8506, the trochlear canal opens into a small recess (Russell 1970), whereas on the right side, the canal penetrates the laterosphenoid without having a secondary structure. Although the larger diameter of the canal alone does not indicate that the nerve was also large, the recess is potentially an attachment site for connective tissues such as the trochlea. These roots of the motor nerves for the extraocular muscles are substantially larger in diameter in CMN 8506 than in those of other tyrannosaurids. In particular, the trochlear passage is narrow in most tyrannosaurid endocasts so that its diameter is smaller than that of the ophthalmic branch (CN V1) (Osborn 1912; Brochu 2000; Saveliev and Alifanov 2007; Witmer and Ridgely 2009, 2010; Bever et al. 2013). This relationship is reversed in CMN 8506, and observation of the original specimen rules out the possibility of reconstruction artifact.
CMN 8506 has an even more unusual trait. The trochlear nerve exits the endocranial cavity preoptically (directly above or anterior to the optic fenestra). In all other tyrannosaurid endocasts including that of TMP 2001.36.1, the trochlear nerve has its root in a postoptic position, dorsal to that of the oculomotor nerve (Osborn 1912; Brochu 2000; Saveliev and Alifanov 2007; Witmer and Ridgely 2009, 2010; Bever et al. 2013). Despite this substantial anterior shift, the external trochlear foramina of CMN 8506 correspond in overall configuration to those of other tyrannosaurids. The trochlear nerves of CMN 8506 probably extended within the endocranial cavity longer than those of other tyrannosaurids, so as to have preoptically shifted internal foramina and shorter endoosseous canals.
Hindbrain and spinal cord
The hindbrain includes the cerebellum and medulla oblongata, and gives rise to CN V–XI. The hypoglossal nerve (CN XII) originates immediately posterior to it (corresponding to the exoccipital part of the otoccipital) at the level of the spinal cord. Like other regions of the brain, the cerebellum cannot be delineated clearly in the endocasts of CMN 8506 and TMP 2001.36.1, but the flocculus indicates its approximate position. The flocculus extends posterolaterally through the loop of the anterior semicircular canal of the inner ear. In both CMN 8506 and TMP 2001.36.1, the flocculus is tongue-like and compressed transversely in cross section. This condition is also observed in mature individuals of Tarbosaurus and Tyrannosaurus (Saveliev and Alifanov 2007; Witmer and Ridgely 2009). In smaller tyrannosaurids such as CMNH 7541 and Gorgosaurus, the flocculus is similarly tongue-like, but extends further posteriorly to the level of crus communis (Witmer and Ridgely 2009, 2010).
In Alioramus, Dilong, and other coelurosaurs in general, the flocculus is oval and subcircular in cross section, and extends well past the anterior semicircular canal and into the loop of the posterior semicircular canal (Currie and Zhao 1993b; Lautenschlager et al. 2012; Bever et al. 2013; Balanoff et al. 2014; King et al. 2020; Kundrát et al. 2020). Generally, the relative size of the flocculus negatively correlates with body size among theropods. The endocasts of large non-coelurosaurian theropods (such as Giganotosaurus, Murusraptor, Sinraptor, and various abelisaurids) each tend to have a small flocculus, whereas the structure is relatively large in those of smaller theropods (such as most coelurosaurs and Sinosaurus) (Franzosa and Rowe 2005; Paulina-Carabajal 2011; Paulina-Carabajal and Currie 2012, 2017; Xing et al. 2014; Paulina-Carabajal and Filippi 2018). The exception may be Allosaurus, as at least one specimen (UUVP 294) has a flocculus that almost extended through both anterior and posterior loops of the semicircular canals (Hopson 1979; Rogers 1998). The medulla oblongata is markedly convex ventrally in both CMN 8506 and TMP 2001.36.1, reflecting the greater midbrain flexure in Daspletosaurus compared with Alioramus, Tarbosaurus, and Tyrannosaurus (Saveliev and Alifanov 2007; Witmer and Ridgely 2010, 2010; Bever et al. 2013), but which is similar to Bistahieversor and Gorgosaurus (Witmer and Ridgely 2009; McKeown et al. 2020).
As in other tyrannosaurids (Bakker et al. 1988; Brochu 2000; Currie 2003a; Witmer and Ridgely 2009), the trigeminal ganglia sat within the endocranial cavity in both CMN 8506 and TMP 2001.36.1. Therefore, the ophthalmic (CN V1) and maxillomandibular (CN V2+3) branches extend as separate passages anteriorly and laterally, respectively. The abducens nerve (CN VI) extends into a canal from the floor of the endocranial cavity, ventral to the root of the maxillomandibular branch. The nerve wraps around the hypophyseal fossa and exits the braincase below the ophthalmic foramen. The facial canal (CN VII) is adjacent to but distinct from the maxillomandibular canal, having its external foramen within the same small recess. The glossopharyngeal, vagus and accessory nerves (CN IX–XI), and the lateral head vein all pass through the internal jugular foramen. The glossopharyngeal nerve has its own canal and external opening posteroventral to the columellar recess. The vagus and accessory nerves and the lateral head vein extend within a separate canal through the metotic strut to the external foramen, which opens near the neck of the occipital condyle. In CMN 8506, the hypoglossal nerve (CN XII) has at least two roots. TMP 2001.36.1 likely shared this condition, but the canals have not yet been delineated clearly. The paired posterior mid-cerebral veins drain from below the base of the dural sinus to the occipital plane.
Inner ear
Tyrannosaurids are broadly similar to each other in inner ear morphology. The labyrinths of CMN 8506 and TMP 2001.36.1 also follow the pattern shared across the clade (Fig. 10). In CMN 8506, the lateral semicircular canal cannot be delineated due to the high-density, iron-rich matrix filling in the inner ear, but the preserved parts of the inner ear are similar to those of TMP 2001.36.1, other tyrannosaurids, and most non-avian theropods. In both CMN 8506 and TMP 2001.36.1, the anterior semicircular canal forms a much larger loop than the posterior canal. Holding the ampullae horizontally, the lagena and crus commune are inclined slightly posterodorsally in CMN 8506 and are both nearly vertical in TMP 2001.36.1. In mature individuals of Tyrannosaurus (AMNH 5029, AMNH 5117), both structures are tilted posterodorsally, whereas they are more vertical in smaller tyrannosaurids, such as CMNH 7541 and Gorgosaurus (ROM 1247) (Witmer and Ridgely 2009, 2010). The fenestra ovalis communicates with the vestibule anteromedially at the saccular level, immediately below the lateral semicircular canal. Reconstruction of the labyrinth of TMP 2001.36.1 also reveals the smaller fenestra pseudorotunda below the larger fenestra ovalis. The lagena is narrow, but the constriction and round terminus in CMN 8506 may be artifacts of reconstruction.
Fig. 10.
CMN 8506 has two unusual characters for a tyrannosaurid in the inner ear. First, the ampulla of the anterior semicircular canal may lack a bulging expansion observed broadly among theropods. This is perhaps a preservational artifact, as the adjoining lateral canal was never reconstructed for this specimen. Second, the lagena is as tall as the anterior semicircular canal, even though, generally, it is markedly shorter than the height of the loop among most theropods (Witmer and Ridgely 2009). Potentially, this character is shared with Alioramus and Bistahieversor (Bever et al. 2013; McKeown et al. 2020). Although missing much of the vertical semicircular canals in NMMNH P-25049, Bistahieversor may also have a tall, inclined lagena (McKeown et al. 2020).
Pneumaticity
The braincases of tyrannosaurids are air filled. CMN 8506 and TMP 2001.36.1 are no exceptions to this (Figs. 5, 6, 11, 12). Diverticula invade tyrannosaurid skull elements regardless of their embryonic origins, axial levels, or dorsoventral/lateromedial depths (Currie and Zhao 1993b; Witmer 1997; Currie 2003a; Witmer and Ridgely 2008, 2009; Gold et al. 2013). Within a braincase, the skull roof is essentially free of pneumatic recesses. The endochondrally ossified, mesoderm-derived elements dominate in the lateral walls and floors of the endocranial cavity, and many of these are highly pneumatized in tyrannosaurids: basioccipital, basisphenoid, laterosphenoid, otoccipital, parasphenoid, prootic, and supraoccipital. A diverticulum often has a specific relationship with a braincase element and, generally, does not cross open sutures. Where a recess pneumatizes multiple braincase elements, each element is associated with a distinct chamber or diverticulum within the recess. These are the anterior tympanic recess invading the laterosphenoid and prootic, the subcondylar recess extending onto the otoccipital from the basioccipital, and the posterior tympanic recess, which excavates the otoccipital (a fused complex of exoccipital and opisthotic), extends into the prootic, and becomes confluent through the supraoccipital dorsomedially.
Fig. 11.
Fig. 12.
There are multiple sources to the diverticula (Hogg 1984, 1990; Witmer and Ridgely 2009; Dufeau and Witmer 2015; Tahara and Larsson 2019a, 2019b). In tyrannosaurid braincases, the anterior and posterior tympanic recesses correspond to those in living birds. These diverticula are each derived from the paratympanic cavity, which is pneumatized by the Eustachian tube (embryonic hyomandibular pouch) (Romanoff 1960; Hogg 1990; Tahara and Larsson 2019a). In tyrannosaurids, the median pharyngeal (basisphenoid, subsellar) systems are likely associated with a median extension from the pharynx (Dufeau and Witmer 2015; Young and Bierman 2019) as the recesses open mid-ventrally. This is consistent with most non-avian theropods and modern crocodiles (Witmer et al. 2008; Dufeau and Witmer 2015). In contrast, the basisphenoid and parasphenoid sinuses are derived from the anterior tympanic diverticulum and closed ventrally by the parasphenoid lamina in birds and troodontids (Saiff 1981, 1982; Witmer 1990; Baumel and Witmer 1993; Currie and Zhao 1993b; Starck 1995; Xu et al. 2002; Vorster and Starck 2003; Norell et al. 2009; Mayr 2020). In a Japanese quail, the left and right diverticula become confluent to pneumatize the basisphenoid and parasphenoid (Tahara and Larsson 2019a). Distinct from these systems, the subcondylar recess has a pneumatopore on the posterior side of the braincase and exclusively pneumatizes the derivative of the sclerotomes of the postotic somites (basioccipitals), which at that stage of development form a series with those that give rise to vertebrae (De Beer 1937; Crompton 1953; Jollie 1957; Romanoff 1960; Vorster 1989). Comparative overviews suggest that the braincase pneumaticity is phylogenetically conservative in overall configuration. However, specific sources of the diverticula may vary between lineages, and some bones are not universally pneumatized across theropods (Saiff 1974, 1978; Hogg 1984; Starck 1995; Currie 1997; Witmer et al. 2008; Tahara and Larsson 2019a, 2019b; Leardi et al. 2020).
Ontogenetically, adjacent air sacs may develop connections through small openings secondarily, regardless of whether or not they are pneumatized by the same main diverticulum. These secondary pneumatic features might not be as strongly controlled within or across species as the primary sinus development. These and other pneumaticity-related characters appear to vary within species and sometimes between the left and right sides of the same braincase, implying that these pneumatic connections may be of limited use for taxonomic distinction. The braincases of Allosaurus from a single bonebed also have high frequencies of variation (Chure and Madsen 1996). In an extreme example of standing variations in the pneumatic connections, the anterior tympanic and subcondylar recesses are broadly confluent in a mature individual of Bistahieversor (NMMNH P-27469) (McKeown et al. 2020), even though the lower portion of the anterior tympanic recess is labeled as part of subcondylar recess in that reconstruction.
Anterior tympanic recess
The anterior tympanic recess has a single pneumatopore under the ala basisphenoidalis, adjacent to the internal carotid foramen (Figs. 5, 6, 11, 12). It pneumatizes the anterodorsal and laterodorsal portions of the basisphenoid, as well as the dorsum sellae, preotic pendant, and otosphenoidal crest. As a result, the recess wraps around the hypophyseal fossa from three sides. The left and right anterior tympanic recesses become confluent behind the hypophyseal fossa, below the ophthalmic and maxillomandibular roots (CN V). This transverse bridge — retrohypophyseal sinus sensu Witmer and Ridgely (2009) — is also confluent with the basisphenoid recess directly beneath it, and it is difficult to delineate contributions from these two different systems. The communication is broader and more extensive in TMP 2001.36.1 than in CMN 8506. As the basicranium becomes taller with the ventral extension of the basipterygoid processes, the transverse bridge between the anterior tympanic recesses also shift more ventrally with respect to the hypophyseal fossa. In Tyrannosaurus, the recesses become confluent behind the hypophyseal fossa in CMNH 7541, and at the level below the hypophyseal fossa in a mature individual (AMNH 5117) (Witmer and Ridgely 2009, 2010). These variations suggest that relative positions of these air sacs and the extent of inter-sinus communications change during the growth of a tyrannosaur, probably in correlation with body size rather than with age or taxonomic distinctions.
In both CMN 8506 and TMP 2001.36.1, a small sinus is present anterior to the retrohypophyseal sinus and ventral to the hypophyseal fossa. This anterior extension of the anterior tympanic recess is the prohypophyseal sinus (sensu Witmer and Ridgely 2009). It is present in CMNH 7541 and Gorgosaurus, but absent in Bistahieversor and, notably, a mature individual of Tyrannosaurus (AMNH 5117) (Witmer and Ridgely 2009; McKeown et al. 2020). The prohypophyseal sinus is better developed in CMN 8506 than in TMP 2001.36.1. In CMN 8506, the prohypophyseal sinus is distinct from the retrohypophyseal sinus and wraps around the bottom of the hypophyseal fossa (Figs. 5A–5C, 5E, 11A–11C, 11E), whereas in TMP 2001.36.1 the same sinus is an incipient anterior outgrowth ventral to the hypophysis (Figs. 6A, 6B, 6E, 12A, 12B, 12E).
The anterior tympanic recess has an ascending diverticulum into the prootic between the trigeminal and facial roots. The ascending diverticulum is a more pronounced, distinct chamber in TMP 2001.36.1 (Figs. 6 and 12), whereas that of CMN 8506 is rudimentary and never extends above the trigeminal and facial roots (Figs. 5 and 11). Alioramus, Gorgosaurus, and CMNH 7541 are more similar to TMP 2001.36.1 in having a well-developed ascending diverticulum (Witmer and Ridgely 2009, 2010; Bever et al. 2013). This diverticulum is absent or weakly developed in mature individuals of Tyrannosaurus (Witmer and Ridgely 2009) as in CMN 8506.
Posterior tympanic recess
As the largest air sac in a tyrannosaur braincase by volume, the posterior tympanic recess pneumatizes the otoccipital and part of the prootic. The main pneumatopore is on the anterolateral surface of the paroccipital process, immediately below the otosphenoidal crest, above the columellar groove, and posterior to the columellar recess (Figs. 5, 6, 11, 12). In Gorgosaurus and Tyrannosaurus, the columella crosses over the pneumatopore (Witmer and Ridgely 2009), although this character likely varies intraspecifically (the pneumatopore opens above the columellar groove in at least one mature specimen of Tyrannosaurus, RSM P2523.8; Persons et al. 2020). Another, smaller pneumatopore exists on the posterodorsal surface of the paroccipital process, medial to the parietal contact. The paroccipital process is entirely pneumatized in TMP 2001.36.1 (on the left side), whereas in CMN 8506, the posterior tympanic recess is restricted to the upper two thirds of the process (both left and right sides). The right paroccipital process of TMP 2001.36.1 is damaged (reconstruction of this region is incomplete), but the process appears to be pneumatized in the lower half where the distal corner of the process is broken. In Alioramus and Tyrannosaurus (AMNH 5117, CMNH 7541), the recess excavates only the upper half of the process, whereas in Bistahieversor and Gorgosaurus, the recess occupies the length and height of the paroccipital process (Witmer and Ridgely 2009, 2010; Bever et al. 2013; McKeown et al. 2020).
The left and right posterior tympanic recesses become confluent through the supraoccipital sinus, just as the left and right anterior tympanic recesses communicate through the retrohypophyseal sinus (Figs. 5, 6, 11, 12) — a feature considered in the context of auditory functions (Currie and Zhao 1993b). The supraoccipital sinus is a distinct chamber within the element bordered by unclosed sutures. It is universally present in tyrannosaurids, but the non-tyrannosaurid tyrannosaur Timurlengia has an apneumatic supraoccipital (Brusatte et al. 2016). In TMP 94.143.1, a thin bony wall incompletely separates the supraoccipital sinus and the posterior tympanic recess. The connection between the supraoccipital sinus and the paroccipital sinus is constricted dorsally by the posterior mid-cerebral vein and ventrally by the jugular (= lateral head) vein (through the vagal canal). The sinus extends dorsally above the foramen magnum to pneumatize the paired supraoccipital knobs. These conditions are broadly present among coelurosaurs (Currie and Zhao 1993b; Witmer and Ridgely 2009; Bever et al. 2013).
Subsellar recess
One of the median pharyngeal air sacs, the subsellar recess sits in the base of the cultriform process in the parasphenoid (Figs. 5, 6, 11, 12). The process is damaged in both CMN 8506 and TMP 2001.36.1 so reconstruction remains incomplete. Based on the preserved regions, the subsellar recess extends dorsally to approach the level of the hypophyseal fossa in TMP 2001.36.1. This is also the case in CMNH 7541 (Witmer and Ridgely 2010). In CMN 8506, the top of the subsellar recess is well below the bottom of the hypophyseal fossa. This separation is greater in a mature individual of Tyrannosaurus (AMNH 5117) (Witmer and Ridgely 2009).
Basisphenoid recess (including basipterygoid recess)
The basisphenoid recess housed a deep median pharyngeal air sac with multiple diverticula (Figs. 5, 6, 11, 12). The aperture of the recess is defined by four corners, which are paired basipterygoid processes and basal tubera. As a broadly observed feature among tyrannosaurids, the massive recess extends dorsally into the endocranial floor to wedge between the anterior tympanic and subcondylar recesses. In CMN 8506, the chamber has paired organization. In TMP 2001.36.1, this may have communication with the anterior tympanic recess. This top region of the basisphenoid recess is reduced or lost in mature individuals of Tyrannosaurus (Witmer and Ridgely 2009), whereas in CMNH 7541, the diverticulum is present and split into paired sinuses dorsally (Witmer and Ridgely 2010). The two specimens of Daspletosaurus clearly show that each of the paired posterodorsal chambers gives rise to a ventrolateral diverticulum that pneumatizes the basisphenoid portion of the basal tuber (diverticulum tuberalis). This condition is also present in Gorgosaurus ROM 1247 (Witmer and Ridgely 2009). Independent of this diverticulum, TMP 2001.36.1 has paired pneumatic diverticula that extend posterodorsally on the lateral walls of the basisphenoid recess (Figs. 6, 12). This clear delineation of the posteroventral edges of the recess appears unique among the specimens considered in this paper.
Anteriorly, tyrannosaurids typically have paired diverticula that pneumatize the interbasipterygoid lamina (Bakker et al. 1988; Witmer and Ridgely 2009). These diverticula extend ventrally into the basipterygoid processes. TMP 2001.36.1 is consistent with this pattern, but CMN 8506 appears to have this diverticulum only on the right side and penetrating the interbasipterygoid lamina in a much lower position than in other tyrannosaurids (Figs. 5, 11). As a result, the basipterygoid recesses are largely distinct paired sinuses clearly separated from the dorsal portion of the basisphenoid recess. The single aperture also occurs on the right side in CMNH 7541, but in this specimen the basipterygoid processes are poorly pneumatized by the recesses (Witmer and Ridgely 2010).
In theropods, the basipterygoid process is pneumatized typically from the lateral side of the braincase in proximity with the anterior tympanic system and the internal carotid artery. The recess may be a depression on the lateral surface of the basipterygoid process (Chure and Madsen 1996; Barsbold and Osmólska 1999; Xu et al. 2002; Rauhut 2004; Norell et al. 2006; Smith et al. 2011) or may have a laterally open pneumatopore behind the preotic pendant (Osmólska et al. 1972; Currie 1985; Makovicky and Norell 1998; Paulina-Carabajal and Currie 2017). Among tyrannosaurids, Alioramus has the latter condition and also shows left–right asymmetry in the pneumatopore morphology (Bever et al. 2013; T. Miyashita, personal observation on PIN 3141-1). Unlike Alioramus, there is no separate external aperture for the basipterygoid recesses in CMN 8506, CMNH 7541, or other tyrannosaurid braincases. Interestingly, Sinraptor also has internal apertures within the basisphenoidal recess, which open into the basipterygoid recess (Paulina-Carabajal and Currie 2012) — a condition otherwise observed in tyrannosaurids. The basipterygoid recess has not been reconstructed for Bistahieversor (McKeown et al. 2020), but it is unclear whether the processes are apneumatic or the sinuses are present but cannot be delineated.
In a further departure from the normal tyrannosaurid pattern, CMN 8506 has a large median aperture in the anterodorsal end of the basisphenoid recess, approximately where the basipterygoid–basisphenoid communications occur in other tyrannosaurids. This aperture has a diverticulum leading to a distinct chamber, anterior to the main basisphenoid recess, dorsal to the subsellar recess, ventral to the prohypophyseal sinus of the anterior tympanic recess (Figs. 5, 11). Although smaller in size, the same sinus is present in TMP 2001.36.1.
Subcondylar recess
The subcondylar system consists of external and internal structures. The homology and terminology of each component remains to be resolved in theropods. Externally, there are a median pneumatic fossa (subcondylar or medial subcondylar) from the base of the occipital condyle to between the basal tubera, and paired lateral pneumatic fossae (paracondylar, lateral subcondylar) that flank the median fossa along the basioccipital–otoccipital suture. Internally, there are medial and lateral sinuses that do not necessarily correspond to the external features in their lateral versus medial terminology. This description focuses on the internal structures hereafter.
In tyrannosaurids including TMP 2001.36.1, the internal subcondylar recess consists of medial and lateral sinuses, each having a pneumatopore within the external lateral fossa at the base of the occipital condyle, near the basioccipital–otoccipital suture, and below the vagal and hypoglossal foramina (Witmer and Ridgely 2009). However, the lateral subcondylar sinus is rudimentary in CMN 8506 (Figs. 5, 11). The medial subcondylar sinus is clearly visible in the same specimen, so it is reasonable to rule out taphonomic or reconstruction artifacts to explain this difference. In CMN 8506, the left and right diverticula entering through the pneumatopores become confluent within a large median recess. The median recess extends as anteriorly as to below the inner ear and occupies greater total volume than the anterior tympanic recess. It has paired lateral wings, which are rudimentary lateral subcondylar sinuses. These small chambers do not seem to cross the basioccipital–otoccipital suture or have their own pneumatopores, although the base of the occipital condyle has been damaged in this specimen.
In TMP 2001.36.1, the medial chamber is relatively small and restricted to the region posterior to the inner ears (Figs. 6, 12). Instead, the recess has paired lateral sinuses that extend far laterally and pneumatize the bases of the paroccipital processes (crista tuberalis). In posterior view, the subcondylar recess has a butterfly shape in TMP 2001.36.1. Tyrannosaurus also has a butterfly-shaped subcondylar recess regardless of age or size because this condition occurs both in AMNH 5117 and CMNH 7541 (Witmer and Ridgely 2009). Although taphonomically compressed, a specimen of Gorgosaurus (ROM 1247) has large lateral subcondylar sinuses as well (Witmer and Ridgely 2009). In these comparative specimens and CMN 8506, the medial sinuses had relatively larger volumes within the subcondylar recess than that in TMP 2001.36.1. In particular, that of CMN 8506 is distinct from other tyrannosaurids by expanding into the large, main chamber of the subcondylar recess.
In TMP 2001.36.1, the medial subcondylar sinus has small paired diverticula extending toward the basioccipital portion of the basal tubera, in parallel to the basioccipital–basisphenoid suture and the diverticulum tuberalis of the basisphenoid recess. These pneumatic extensions are present in Gorgosaurus and Tyrannosaurus (Witmer and Ridgely 2009) but do not seem to extend nearly as ventrally toward the basal tubera as in TMP 2001.36.1. No such distinct diverticulum is described in Alioramus or Bistahieversor (Bever et al. 2013; McKeown et al. 2020). Instead, the basal tuber is pneumatized in these taxa by what corresponds to the lateral sinus of the subcondylar recess in TMP 2001.36.1. In a departure from all these forms, CMN 8506 does not have a diverticulum that extends ventrally beyond the pneumatopore (Figs. 5, 11). Therefore, the diverticulum tuberalis is interpreted as absent for the subcondylar recess in this specimen.
As in the connections between the anterior tympanic and basisphenoid recesses, the subcondylar recess can also communicate with adjacent pneumatic spaces derived from different diverticula. In all but one known braincase of a tyrannosaurid (CMN 8506), the lateral subcondylar sinus pneumatizes the metotic strut (Russell 1970; Witmer and Ridgely 2009). Interestingly, the lateral subcondylar sinus communicates with the posterior tympanic recess dorsally on the left side of the braincase of TMP 2001.36.1, although an extent of the communication is unclear on the right side (Figs. 6A–6C, 6F, 12A–12C, 12F; colour coded as green to highlight the boundary between the medial and lateral sinuses). The same region in CMN 8506 appears to have no extensive pneumatization (Figs. 5, 11). In Bistahieversor (NMMNH P-27469), the lateral sinuses are so well developed that they not only pneumatize bases of the paroccipital process but become broadly continuous with the anterior tympanic recess (McKeown et al. 2020). Although it cannot be ruled out that these adjacent pneumatic systems developed diverticula to replace the lateral subcondylar sinuses, a conservative approach is to treat these as secondarily modified inter-sinus communications.
Discussion
Braincases are often assumed to be anatomically conservative (Currie 1985, 1997; Currie and Zhao 1993b; Paulina-Carabajal 2011). However, specific rationales behind this assumption are sometimes ignored. Braincases and endocasts are anatomically conservative in that: (i) brain regions, cranial nerves, and sensory capsules are broadly homologous across vertebrates; (ii) these tissues often have specific relationships with the surrounding bones and cartilages; and (iii) the resulting, evolutionarily conserved patterns provide landmarks for homology of the peripheral structures, including cranial circulation and musculature. Therefore, there is little reason to believe that braincase anatomy is any more conservative than other parts of a skull within and between species, apart from these broadly conserved, pan-vertebrate/gnathostome patterns.
Unfortunately, the internalized parts like braincases are often inaccessible in otherwise well-preserved skulls. Sample size is typically small, and it is rare for a taxon to have more than one or two complete braincases with extensive information available on internal features. As such, the taxa available for a comparison of braincase characters tend to be few and phylogenetically wide apart, and polymorphism within a taxon, if any, cannot be detected. These biases conflate the assumption of general conservatism in braincase anatomy, and can also lead to an artifact where degrees of variation appear uneven in different parts of the tree. For example, variation among tyrannosauroid braincases has been set in a “zone of variability” against non-detection of similar variation in non-coelurosaur theropods and maniraptoriforms (Bever et al. 2011). As discussed later in the context of tyrannosaurid braincases, a zone of variability (Bever et al. 2011) is essentially a non-falsifiable concept for several reasons: (i) its theoretical premises are arbitrary and lacking scale (it broadly assumes that microevolutionary process cascades to macroevolutionary pattern, and that variation in morphology is linked to that of developmental pathways; it also compares terminal states to node states); (ii) it does not discriminate observational artifacts (uneven sampling); and (iii) designating a zone of variability based on observed frequencies of variation is self-confirmatory.
Tyrannosaurids offer an important data set with which to test the assumption of conservatism at multiple levels. A handful of anatomically similar members of this clade are known from multiple well-preserved braincases, and in some of these taxa different ages and sizes are represented (Albertosaurus, Daspletosaurus, Gorgosaurus, Tarbosaurus, and Tyrannosaurus). The path-breaking work on Tyrannosaurus by Witmer and Ridgely (2009) revealed high degrees of variation in braincase anatomy within Tyrannosaurus (denoted by “§” in Table 1). Some of these characters, as discussed in Witmer and Ridgely (2009) and this paper, are likely correlates of body size and age (denoted by “∗” in Table 1). These include degrees of ossification, and relative proportions of soft structures identified in the endocasts and pneumatic recesses. However, some traits appear to vary within species, independent of body size, and potentially at the individual level. These characters are identified in the endocasts and pneumatic recesses, as well as the external bone morphology. In addition to this, the recently published character data set on skeletal variation in Tyrannosaurus include numerous variations on external braincase morphology (Carr 2020). As these latter variations are mainly correlates of age and size recorded within a single taxon (and as a large number of the characters cited by Carr (2020) are redundant with each other), they are not listed here in the interspecific context. Because all taxa in Table 1 except Tyrannosaurus are mainly compared on the basis of a single specimen, the extent of polymorphic characters as discussed in this paper is grossly underestimated.
Table 1.
With or without intraspecific variations, a number of characters are useful correlates of taxonomic distinction. The clearest examples are those expressed independent of body size differences (ala basisphenoidalis, lagenar height, midbrain flexure, paroccipital process, pneumatopore of posterior tympanic recess, subcondylar recess: Table 1). Some other characters have likely autapomorphic states identified in CMN 8506 (basal tuber with a well-defined neck, preoptically shifted passage for the trochlear nerve, long common carotid canal, narrow ampulla of anterior semicircular canal, distinct anterodorsal chamber of basisphenoid recess). Table 1 also lists characters that vary within and among species but which are independent of body size, and have some indications for a representative state within the taxon (basipterygoid–basisphenoid recesses, dural peak, hypophysis, olfactory tract, sagittal crest, trochlear root). Conversely, there are characters that vary among taxa but partly correlate with body size differences (ascending diverticulum of anterior tympanic recess, lagenar orientation, crista tuberalis, flocculus, subsellar recess, suture development: Table 1). These variations are taxonomically useful when compared among similarly sized specimens. In principle, variations are not listed in Table 1 if they do not differ in character states between CMN 8506 and TMP 2001.36.1. As discussed in the description, many of these excluded characters are taxonomically informative for tyrannosaurids in general (e.g., basisphenoid orientations, frontal–parietal suture, height of nuchal crest, sagittal peak of interfrontal suture).
The results of this description are consistent with other descriptive studies of tyrannosaurid braincases in documenting high degrees of variation in both the endocasts and pneumatic systems (Russell 1970; Bakker et al. 1988; Currie 2003a; Currie et al. 2003; Witmer and Ridgely 2009, 2010; Bever et al. 2013; McKeown et al. 2020). A large number of character variations in the endocasts seem surprising, but these variations likely reflect the changing relationships between the endocranial cavity and brain across great magnitudes of body size differences, rather than changes in the brain morphology itself. A high degree of variation in the pneumatic systems have been long recognized in the literature. These variations have allometric, individual, ontogenetic, and taxonomic correlates, and no single pattern can explain the variations overall.
Based on the information from Tyrannosaurus (Witmer and Ridgely 2009, 2010), McKeown et al. (2020) predicted shortening of the lagena and a general decrease in the pneumaticity across the growth of a tyrannosaurid. These proposed ontogenetic changes assume allometric trends, but the lagenar proportions do not fit the purported trend exactly as Gorgosaurus has a relatively short lagena (Witmer and Ridgely 2009). As for the pneumaticity, many of the predicted trends (e.g., reduction of prohypophyseal sinus and ascending column of anterior tympanic recess; loss of paroccipital–subcondylar connection) are difficult to generalize across a size series of tyrannosaurids because the juvenile conditions presumed by McKeown et al. (2020) are underpinned by a single specimen (CMNH 7541). McKeown et al. (2020) link ossification during the growth and relative loss of the pneumaticity, but these processes need not be so tightly coupled. The sinuses may expand and new connections may form stochastically as skeletal remodeling processes resorb the bone (Hogg 1990; Dufeau and Witmer 2015; Tahara and Larsson 2019a). Because of the three-dimensional profiles of the sinuses, relative air volumes would increase, not decrease, against the increasing linear dimensions of the braincase. It is more reasonable to consider the pneumatic systems as ontogenetically dynamic, changing their forms as skeletal growth and remodeling modify shapes, dimensions, and mechanical loading of the braincases.
In the context of this paper, those characters that differ between CMN 8506 and TMP 2001.36.1 are of particular interest (Table 1). Given intraspecific variations in Gorgosaurus and Tyrannosaurus, suture development and subsellar recess have little systematic utility. CMN 8506 shows potentially autapomorphic characters of Daspletosaurus torosus. These are the well-developed basal tuber, the large and distinct anterodorsal chamber of the basisphenoid recess, the preoptically shifted root of the trochlear nerve, the long, posteroventrally inclined common carotid canal, the subcondylar recess with a large median sinus and reduced lateral sinuses (also lacking a diverticulum to the basal tuber), the asymmetric aperture and distinct basipterygoid recess (partly overlapped with CMNH 7541), and the rudimentary ascending column of the anterior tympanic recess (at large body size). The narrow ampulla of the anterior semicircular canal and the vertical hypophysis in CMN 8506 could also be listed, but reconstruction artifact cannot be ruled out. The low basioccipital profile is unique among large-bodied tyrannosaurines, even though this character state is shared with relatively small individuals (CMNH 7541, ROM 1247). The robust oculomotor and trochlear canals in CMN 8506 are unique, but it is likely that these represent abnormal conditions rather than characterize this taxon.
Similarly, TMP 2001.36.1 has traits that potentially distinguish it from Daspletosaurus torosus. These include the paired sinuses on the lateral wall of the basisphenoid recess (likely unique among tyrannosaurids), the short, vertical lagena (unique among tyrannosaurines), the entirely pneumatized paroccipital process (shared with Bistahieversor and Gorgosaurus), the well-developed crista tuberalis (at large body size; shared with Bistahieversor and Tyrannosaurus), and the curved ala basisphenoidalis (shared with both Gorgosaurus and Tyrannosaurus). The bottlenecked olfactory tract in TMP 2001.36.1 represents an interesting departure, because this character state occurs mainly in smaller tyrannosaurids (shared with Alioramus, Bistahieversor, and Gorgosaurus). Although variable within Daspletosaurus sp, the thick sagittal crest in TMP 2001.36.1 and the laterosphenoid–sphenethmoid contact in CMN 1184 can potentially be used to set apart the two species. Except for the basipterygoid–basisphenoid recesses, communications between the pneumatic sinuses are excluded from Table 1 because of high frequencies of variation at the level of individuals and sometimes between contralateral sides.
Conversely, the characters that have similar states in both CMN 8506 and TMP 2001.36.1 may be useful to distinguish the genus Daspletosaurus from other tyrannosaurids (Table 1). These candidates include a deep midbrain flexure, the presence of an anterodorsal chamber of the basisphenoid recess (regardless of size variation), and the presence of a prohypophyseal sinus of the anterior tympanic recess at large body size. However, it is challenging to rule out allometric or individual variation for these characters. This will be a subject of the future study that will draw from a larger data set.
This description serves as a primer for broader and detailed comparison. Only two specimens (one each for two species) are described in this paper, and only a handful of specimens outside Daspletosaurus are used for comparison. The characters, including those expressed differently between CMN 8506 and TMP 2001.36.1, require a further analysis to determine how they vary within and across species before a diagnosis is formulated. Allometric/ontogenetic trends and phylogenetic implications also remain to be explored using quantitative methods. These are beyond the scope of this paper and the subjects of the ongoing work on Daspletosaurus by the second and last authors.
Outgroup selection remains as a challenge for a comparative analysis of tyrannosaurid braincases. Dilong, Guanlong, Stokesosaurus, Timurlengia, Xiongguanlong, and potentially Yutyrannus provide information for external braincase morphology and some internal reconstructions (Chure and Madsen 1998; Xu et al. 2004, 2006, 2012; Li et al. 2010; Brusatte et al. 2016; Kundrát et al. 2020). Beyond tyrannosauroids, Ornithomimus is the phylogenetically closest plesiomorphic taxon published with extensive internal reconstruction (Tahara and Larsson 2011). The endocranial anatomy of multiple oviraptorosaurs and therizinosauroids have been recently reconstructed (Kundrát 2007; Kundrát and Janáček 2007; Balanoff et al. 2009, 2014, 2018; Smith et al. 2011, 2018; Lautenschlager et al. 2012; Balanoff and Norell 2012; Smith 2014), but they represent highly modified coelurosaur conditions. Without this recent progress, tyrannosaurids would appear to have markedly greater variation in braincase morphology than other theropod lineages (Bever et al. 2011) by the virtue of simply having more taxa with reconstructed braincases within tyrannosaurids than in each of other comparative clades. However, this purportedly high variation is likely an artifact of uneven sampling.
Russell (1970) was the first to recognize taxonomic significance in variation of braincase morphology — particularly that of braincase pneumaticity — among tyrannosaurids. Specifically in regard to Daspletosaurus, the characters he used to diagnose the genus are now considered to be either non-diagnostic (basisphenoid recess situated midline and bordered by interbasipterygoid lamina, optic fenestra (CN II) undivided, and ophthalmic foramen (CN V1) on laterosphenoid) or misidentifications (Russell considered that oculomotor and trochlear nerves (CN III and CN IV) shared a single pit, but these two nerves have separate foramina). However, the choice of the characters clearly reflects Russell’s vision of tyrannosaurid braincases not as a static but as a dynamic system. Russell’s insight leaves a mark on the next important treatment of tyrannosaurid braincases by Bakker et al. (1988) who compared the basicranial traits, especially those of the basisphenoid recess, across tyrannosaurids in great detail. This line of work has culminated in a study by Witmer and Ridgely (2009) that laid the foundation for subsequent comparative analyses, including not only this paper but those by Witmer and Ridgely (2010), Bever et al. (2013), and McKeown et al. (2020), all of which tend to focus on specific taxa or specimens. The series of works represents one of many lines of inquiry about tyrannosaurids that Russell (1970) pioneered. With many questions left to explore about the tyrannosaurid braincases, Russell’s legacy continues to shape and guide the current and future research on these massive yet hollow, intricately complex structures.
Acknowledgements
The authors thank Jordan Mallon and Kathlyn Stewart for inviting this contribution and patiently guiding it to completion; Canada Diagnostic Center and Montfort Hospital for performing CT scans; Brandon Strilisky and James Gardner (TMP) and Kieran Shepherd (CMN) for providing access to TMP 2001.36.1 and CMN 8506, respectively; Tom Courtney, Susan Sabrowski, Shayda Spakowski (TMP), Margaret Currie, Alan MacDonald, and Susan Swan (CMN) for assistance in the respective collections; Laura Shychoski for data acquisition on TMP 2001.36.1; Jordan Mallon and Michael Ryan for data acquisition on CMN 8506; and Bradley McFeeters and an anonymous reviewer for comments. Author contributions: P.J.C. led the field collection of TMP 2001.36.1 and designed the project; A.P.C. scanned and reconstructed TMP 2001.36.1; H.C.E.L. scanned and prepared the preliminary reconstruction of CMN 8506; T.W.D. and T.M. reconstructed CMN 8506; T.M., A.P.C., and P.J.C. analyzed data; A.P.C., T.M., and T.W.D. prepared figures; T.M. wrote the manuscript with input from A.P.C., P.J.C., and H.C.E.L.
Footnote
2
Supplementary data are available with the article at https://doi.org/10.1139/cjes-2020-0185.
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Canadian Journal of Earth Sciences
Volume 58 • Number 9 • September 2021
Pages: 885 - 910
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Received: 29 September 2020
Accepted: 9 March 2021
Published online: 19 August 2021
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Ariana Paulina Carabajal, Philip J. Currie, Thomas W. Dudgeon, Hans C.E. Larsson, and Tetsuto Miyashita. 2021. Two braincases of Daspletosaurus (Theropoda: Tyrannosauridae): anatomy and comparison1. Canadian Journal of Earth Sciences.
58(9): 885-910. https://doi.org/10.1139/cjes-2020-0185
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