The epipterygoid of crocodyliforms and its significance for the evolution of the orbitotemporal region of eusuchians
C. M. Holliday and L. M. Witmer. 2009. Journal of Vertebrate Paleontology 29(3):715-733.
Transgression and vestiges of the epipterygoid in crocodilian skulls
Crocodyliforms (fossil and extant crocodilians) have a long, complicated, and incredibly interesting, albeit still underrated, history. Their snout shapes, toothy grins, and large sizes are often the features that capture the attention of scientists, however much about their skulls still remains unknown. One of the key characteristics of the crocodilian skull is that they sutured the palate to the braincase, thereby locking the cranium together (similar to mammals and turtles) in a way that increases their ability to generate massive bite forces, as well as twist their prey apart, and live a life subaquatic. But little is actually known about what happened to key features of the palate after this major transition, namely, what happened to the epipterygoid?
The epipterygoid is the ascending process of the palatoquadrate and plays a major role in the temporal region of almost all tetrapods, including amphibians, turtles, lizards, and non-avian dinosaurs (birds similarly lost the elements) and then also mammals—although mammalian scientists call the element the alisphenoid, or squamous portion of the temporal bone. Particular muscles attach to the element, and the epipterygoid acts as a relatively mobile strut linking the palate to the skull roof and braincase of lizards, dinosaurs, as well as the fossil relatives of crocs.
Living crocodilians don't have an epipterygoid, but the fossil relatives of crocodyliforms do (e.g., sphenosuchians). Changes in the epipterygoid and lateral wall of the braincase likely had a major influence on jaw muscle and trigeminal nerve evolution (see Holliday and Witmer, 2007), and major morphological changes such as this should provide new data to better understand crocodyliform phylogeny.
Here we present a lengthy survey detailing the changes in the morphology and the eventual loss of the epipterygoid among fossil crocodyliforms. Surprisingly, the element persist as a vestigial structure all the way up into the fossil relatives of extant crocs (eusuchians), and can even be found in embryonic Alligator. But this evolutionary picture remains hazy because fossil relatives of gharials, crocodiles, and alligators all appear to possess the element, albeit reduced, suggesting each extant group may have independently lost the element. This gradual shift in morphology likely impacted the topology of the trigeminal nerve, surrounding soft tissues, like jaw muscles, and actually led to a morphologically convergent, though not homologous temporal regoin built by portions of the braincase (i.e., laterosphenoid) rather than by the palate (i.e., epipterygoid).
So, despite some radical changes in the skulls of crocodyliforms, including palatal suturing, changes associated with different feeding behaviors, and subsequent impacts on skull shapes, it took quite a long time to finally eliminate the epipterygoid, which remained in the skull as a vestigial structure among crocodylians of the early Cenozoic (and perhaps more recently).
|Funded by: National Science Foundation: IBN-0407735, IBN-9601174, IOB-0343744; Contract grant sponsors: The Jurassic Foundation; UCMP Sam Welles Fund; Society of Vertebrate Paleontology; OU Student Enhancement Award; OU Graduate Student Senate; OU Departments of Biological and Biomedical Sciences; Marshall University, University of Missour Department of Pathology and Anatomical Sciences.|
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|FIGURE 1. Important soft and bony structures in the orbitotemporal region of basal archosaurs and extant crocodylians. A, CT-based image of skull of the basal suchian Gracilisuchus (MCZ 4117) in left lateral view depicting location of coronal section used in B; schematic of basal archosaur in left lateral view identifying location of D. B, general cranial spaces and bones of interest in left rostral view of axial section of head through the trigeminal foramen caudal to the epipterygoid of basal archosaur; C, relevant soft tissues (nerves, muscles, arteries), same view as B; D, schematic of palate and laterosphenoid with relevant soft tissues in left lateral view E, CT-based image of head of Alligator in left lateral view depicting location of axial section used in B; F, relevant soft tissues (nerves, muscles, arteries) in the extant crocodylian condition, same view as C; G, schematic of palate and laterosphenoid with relevant soft tissues, same view as D.||FIGURE 2. Phylogenetic framework of major clades and taxa of interest discussed in the text based on Larsson and Sues (2007).||FIGURE 3. Overview of relevant osteological structures in extant crocodylians (e.g., Alligator mississippiensis OUVC 9640). A, Alligator skull in left ventrolateral view; B, left ventrolateral view of orbitotemporal region highlighting areas of jaw muscle attachment, osteological correlates, and cranial bones. Illustration courtesy of R. Ridgely.|
Variation in the trigeminal nerves and relevant structures
in extant crocodylians. A, common morphology of the soft
tissues and trigeminal foramen in the crocodylid
||FIGURE 5. Orbitotemporal regions of the rauisuchian Saurosuchus galilei (PVSJ 32) and the protosuchian Protosuchus richardsoni (MCZ 6727) illustrated with CT data. A, dorsal and left lateral views of the skull of Saurosuchus showing location of oblique, parasagittal section; B, left lateral view of palate and braincase of Saurosuchus; C, left lateral and ventral views of Protosuchus showing location of section and inset, and ventral view of horizontal section; D, ventral view of dorsal half of skull showing ventral surfaces of laterosphenoids and epipterygoids in Protosuchus showing epipterygoid; E, interpretive illustration of D.||FIGURE 6. Orbitotemporal region and epipterygoid fossa of the mesoeucrocodylian Pelagosaurus typus. A, left lateral view of BMNH R32599 (CT-based surface) illustrating region of interest; B, orbitotemporal region of BMNH R32599; C, left lateral view of BRLSI M1413 illustrating location of slice in D; D, horizontal section through orbitotemporal region at the level of the trigeminal foramen in BRLSI M1413; E, F, schematics of Pelagosaurus as in Figure 1.|
|FIGURE 7. The orbitotemporal regions and epipterygoid of mesoeucrocodylians in left oblique lateral views. A, Simosuchus clarki (UA 8679) showing broken epipterygoid and relevant structures in left oblique rostrolateral view; B, Araripesuchus sp. (AMNH 24450) showing waisted epipterygoid and relevant structures. C, D, schematics of orbitotemporal regions of specimens as in Figure 1.||FIGURE 8. Orbitotemporal region of the neosuchian Sarcosuchus imperator (MNN 604). A, reference photo of specimen indicating temporal region; B, photograph of temporal region in left lateral view with in situ large, triradiate epipterygoid overlapping the laterosphenoid and covering the trigeminal foramen. C, illustration of orbitotemporal region in left lateral view. D, E, schematics of Sarcosuchus as in Figure 1.||FIGURE 9. Orbitotemporal regions of the dyrosaur cf. Rhabdognathus and the sebecid Hamadasuchus rebouli. A, reference image based on CT data of cf. Rhabdognathus in left lateral view indicating temporal region; B, illustration of the orbitotemporal region of cf. Rhabdognathus (CNRST-SUNY-190) illustrating neuromuscular osteological correlates and epipterygoid fossa in left lateral view; C, reference image based on CT data of Hamadasuchus (ROM 52620) in right lateral view, indicating temporal region; D, Photograph of isolated Hamadasuchus braincase (ROM 54511) indicating epipterygoid, lateral bridge, and other orbitotemporal structures in right ventrolateral view.|
|FIGURE 10. Orbitotemporal regions of the neosuchians Goniopholis lucasii and Eutretauranosuchus illustrating isolated epipterygoid sutured to postorbital process of laterosphenoid. A, illustration of orbitotemporal region of Goniopholis (AMNH 5782) in left ventrolateral view; B, photograph of orbitotemporal region of Eutretauranosuchus (CMNH 8208) in left ventrolateral view indicating fragment of epipterygoid; C, D, schematics of isolated epipterygoid morphotype present in Goniopholis, Eutretauranosuchus, and Hamadasuchus as in Figure 1.||FIGURE 11. Orbitotemporal region of the eusuchian Leidyosuchus canadensis and Eosuchus minor. A, reference image based on CT data of Leidyosuchus (ROM 1903) in left ventrolateral view and photograph of CMN 8942; B, illustration of Leidyosuchus (CMN 8942) in left ventrolateral view illustrating neurovascular osteological correlates, epipterygoid, and lateral bridge of the laterosphenoid. C, D, schematics of isolated epipterygoid morphotype present in Leidyosuchus as in Figure 1; E, reference image of Eosuchus minor (USMN 181577) in ventral view and photograph of right orbitotemporal region in right ventral view showing isolated epipterygoid and laterosphenoid. Specimen is dorsoventrally compressed; F, illustration of right orbitotemporal region highlighting isolated epipterygoid; G, H, schematics of isolated epipterygoid morphotype present in Eosuchus as in Figure 1.||FIGURE 12. Orbitotemporal region of the eusuchian Gryposuchus columbianus (UCMP 38358) illustrating neurovascular osteological correlates and absence of epipterygoid-related features. A, illustration of orbitotemporal region in left lateral view; B, C, schematics of isolated epipterygoid morphotype present in Gryposuchus as in Figure 1.|
|FIGURE 13. Evolution of the epipterygoid, laterosphenoid, and orbitotemporal region in mesoeucrocodylians. A, cladogram of representative non-eusuchian crocodyliform taxa illustrating major character transitions in the orbitotemporal region during crocodilian evolution. B, C, summary of schematics of focal taxa as in Figure 1. Clades: 1, Crocodylomorpha; 2, Mesoeucrocodylia; 3, Neosuchia.||FIGURE 14. Evolution of the epipterygoid and the laterosphenoid of eusuchians. A, shared features in the orbitotemporal regions of extant crocodylians; B, relevant character states mapped on eusuchian phylogeny of Brochu (1997, 1999) and Wu et al. (2001). C, Epipterygoid loss mapped on two competing phylogenies of crocodylian evolution. Left tree, topology from McAliley et al. (2006); right tree, topology from Figure 14B. Epipterygoids are hypothesized to be present in stem eusuchians; D, same as C, except epipterygoids are hypothesized to be absent in stem eusuchians. Clades of interest: 1, Eusuchia; 2, Crocodylia; 3, Gavialoidea; 4, Brevirostres; 5, Crocodyloidea; 6, Alligatoroidea.*, white stars and circles illustrate the second of the two equallyparsimonious character transformations.||FIGURE 15. Reconstructed jaw muscle attachments and trigeminal nerve branches in mesoeucrocodylians that exhibit the focal epipterygoid morphotypes discussed in analysis. Illustrations are from previous figures. A, Pelagosaurus (with epipterygoid reconstructed); B, Sarcosuchus; C, Leidyosuchus.|