Paedotherium

MacPhee, R. D. E., 2014, The Serrialis Bone, Interparietals, “ X ” Elements, Entotympanics, And The Composition Of The Notoungulate Caudal Cranium, Bulletin of the American Museum of Natural History 2014 (384), pp. 1-69 : 1-69

Paedotherium

Despite the derived nature of Pachyrukhinae, the three specimens (AMNH-VP 45914, MLP 52-IX-28-29, and MLP unnumbered2) on which this section is chiefly based provide excellent insights into the morphology of the hegetotherioid caudal cranium. As in the case of the other specimens reviewed in this paper, all are fully adult.

The existence of unexpected elements cannot be discounted merely because their distinctiveness is hard to establish in the adult stage. This is particularly important to emphasize in the case of pachyrukhines, because in these hegetotherioids conditions are complicated. At first glance the squamous portion of the squamosal appears to be reduced to an insignificant rod, the squamosal bar, and thus seems an unlikely source for the thecal covering. In fact, the rostral part of the squamosal is directly connected to the caudal cranium at only one place, the tiny area of continuity between the squamosal bar and the rostral thecal wall (fig. 8D). Sections support this impression (fig. 12A, C). Although frequently broken in specimens, this area of continuity is not the site of a detectable suture (fused or otherwise) and is no wider than the bar itself, i.e., ~ 2 mm. To explain how such remarkably derived conditions may nevertheless conform to those found in other notoungulates requires considerable morphological exploration and comparisons with other placentals with similarly modified squamosals, provided in the rest of this section.

Pachyrukhine notoungulates are chiefly famous for their remarkable morphological and presumed ecological convergence on certain members of Glires, particularly certain leporids and caviomorphs ( Sinclair, 1909; Kraglievich, 1936; Scott, 1937; Cifelli, 1985; Dozo, 1996, 1997; Reguero et al., 2007). Leporid similarities are especially noteworthy and include such features as the long, narrow rostrum bearing lateral rarefactions, lengthy diastemata, markedly hypsodont/hypselodont cheek teeth, ever-growing incisors, voluminous orbits, basicranial kyphosis, persistent fontanelles or cranial hiatuses, deep mandibular ascending rami, highly reduced and barlike squamous portion of the squamosal, and possible leaping adaptations ( Sinclair, 1909; Scott, 1937; Cerdeño and Bond, 1998; Cassini et al., 2010).

A previously unexplored example of leporid/ pachyrukhine convergence—the presence of a potential intracranial joint (ICJ)—has, on investigation, turned out to be basic to the proper interpretation of the pachyrukhine caudal cranium. The existence of an ICJ in certain lagomorphs (e.g., jackrabbit, Lepus californicus ) was first hypothesized by Bramble (1989), who pointed out that, in the midcranial area, a complex of aligned sutural and synchondrosial dense connective tissues intervenes between bone territories in such a way that bone-on-bone contact within the joint is minimized. Providing a kind of syndesmotic “O-ring” of soft tissues, this arrangement divides the skull into two functional moieties: the rostral, comprising all the elements lying in advance of a semicoronal plane through the sphenooccipital synchondrosis, and the caudal, comprising the rear part of the cranium together with the auditory regions. In L. californicus there is probably very little actual movement at the ICJ; its actual purpose, as

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inferred by Bramble (1989), is to act as part of a shock-absorbing apparatus to prevent deformation of the orbits (and therefore visual impairment) during the strike phase of ballistic leaping (see also Stott et al., 2010). On the other hand, short-limbed, nonleaping Ochotona has some of the osteological correlates noted above for Lepus in even more exaggerated form (see Wible, 2007), but with much larger paratympanic spaces, suggesting isolation of the auditory apparatus may also be significant for other reasons as well.

Regardless of putative ICJ function, the alignment of relevant sutures, synchondroses, and hiatuses in pachyrukhines is certainly similar

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been confirmed in pachyrukhine bullae and is thus omitted (see text). Paroccipital process is largely missing; reconstructed outline based on AMNH-VP 45914 (fig. 8B; note differences in position of petrotympanoexoccipital suture in these two specimens). The numerous vascular foramina punctuating dorsal part of auditory bulla are of uncertain homology. In B, double asterisks identify major vascular grooves. Note rugose sutural surfaces for supraoccipital and parietal on medial aspect of theca. Large black arrow is situated in transverse dehiscence between tentorium and medial thecal wall, connecting transverse sulcus with posttemporal canal (not preserved). Note large, pillarlike petrosal crest, which contributes to tentorium .

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enough to their leporid counterparts to make comparison worthwhile (cf. figs. 8–9 and fig. 18). Sutures concerns us first. Immediately subjacent to the mandibular fossa the squamosal and alisphenoid form a delicate preotic flange of bone (not to be confused with the preotic crest, a quite different feature found in some placentals; MacPhee, 1981). In well-preserved Paedotherium fossils this flange touches, but is not fused to, the surface of the auditory bulla. (The flange in the specimen depicted in figure 8B is somewhat damaged.) Although it barely qualifies as such, topologically the contact between flange and bulla can be described as comprising the glaserian fissure in this taxon. Termination of the preotic part of the squamosal at the glaserian fissure would normally mean that the squamosal does not contribute to structures lying directly caudal to this point, such as the epitympanic theca.

In pachyrukhines the epitympanic sinus is so large that it bulges caudally as well as dorsally, and this has several morphological consequences. Virtual sections and microscopic examination of specimens establish that no bones other than the squamosal and petrotympanic directly face onto the airspace within the theca. However, the sutural picture is made complex by the growth of wings or alae from various elements that slightly overlap the swollen thecal walls as well as nearby structures (figs. 12B–E). This is particularly evident in the case of alae developed from the petrosal (or petrotympanic), producing a far greater caudal exposure of this element than is typical for notoungulates (cf. Cochilius , fig. 13; Billet, 2011).

On the dorsal aspect of the skull (fig. 8C, D), the theca enters into sutural relationships with the other bones in the caudal cranium (supraoccipital, parietal, and interparietal). As all relevant sutures are patent in the available material, it is certain that these other bones are separate from, and therefore do not contribute to, the thecal walls. Sutural contacts continue onto the caudal surface of the cranium, between the rear of the auditory region and divisions of the occipital (including the interparietal, which is partly fused to the supraoccipital; see Interparietal Complex). Endocranially (fig. 9B), the exoccipital is in lengthy sutural contact with the petrotympanic, and the medial and lateral ends of the tentorial process of the supraoccipital articulate with the petrosal crest (figs. 11D, 12C). All of these elements are firmly locked together but only weakly joined to the rest of the skull along the caudal perimeter of the ICJ.

Returning to the midcranial region, it may be noted that bone-to-bone contacts are interrupted by two lengthy gaps, denoted here as the piriform fenestra and the dorsal midcranial hiatus (fig. 8A, B). The mammalian piriform fenestra as defined by MacPhee (1981) is present in adult stages of many groups, although it varies greatly in size and conformation ( Wible, 2007). In Paedotherium the outlet for the mandibular nerve (foramen ovale) is not separable osteologically from the larger piriform fenestra; this joint aperture is sometimes identified as the sphenotympanic fissure ( Gabbert, 2004), but here their theoretically separate identities will be maintained. The fenestra is typically positioned, i.e., on the basicranial floor, lateral to the central stem and sandwiched between the auditory region caudally and preotic portions of the alisphenoid and squamosal rostrally.

The dorsal midcranial hiatus is the much larger vacuity situated on the dorsolateral aspect of the skull between the preotic flange and the squamosal bar (fig. 8B, D). Roth (1903) did not describe the hiatus as such, although it can be clearly made out in his illustration of the skull of Pachyrukhos (fig. 3). Significantly, he showed the hiatus as bounded dorsomedially by his “sutura squamoso-mastoidea,” the existence of which comprises his principal evidence for inferring that another, nonsquamosal element must cover the epitympanic theca. Although Roth doubtless had several pachyrukhines to examine, the one depicted in his plate is misleading: as may be seen by comparing figures 3 and 8D, the indicated suture is actually the one between the parietal and the theca, the squamosal bar having been lost in his specimen. (This may or may not

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asterisks,?vascular conduit of uncertain homology, traveling within mastoid canaliculus. The dorsal hiatal

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ridge appears twice in this section, curving across rostrolateral aspect of theca. In B, single black asterisk identifies adital margin of tegmen tympani. Tympanostyloid has retained ontogenetic connection with tegmen tympani, despite sculpturing effects of massive middle ear pneumatization. In C, discontinuity seen in squamosal bar is a fracture, not a suture. Note small vertical septum running between tympanic floor and cochlear prom-

ontorium. In D, white asterisks in transverse sinus and its tributaries. Note extensive fracturing of petrosal.

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be the same specimen as the one figured by Lydekker [1893: pl. 1], who thought the squamosal bar was part of the parietal. Simpson (1936) probably could not have fathomed any of this from the accounts of these authors, and these misidentifications must have added to his overall frustration.)

Despite Roth’s (1903) inadequate descriptions, it is important to consider whether the dorsal hiatus, given its very large size in pachyrukhines, might have held an element, or part of an element, during life. This possibility is nominally suggested by the presence of the low, rugose, dorsal hiatal ridge on the rostral surface of the thecal wall (figs. 8B, 9A). The ridge is denticulated like a typical cranial sutural margin, although less so than (for example) the suture formed between the theca and supraoccipital (figs. 9B, 11D). It runs in a tight, downturning arc from the position of (and in the same convex plane as) the squamosal bar and ends facing on (and in the same convex plane as) the preotic ends of the alisphenoid and squamosal. The fact that these features are oriented in such a specific way strongly implies that something stretched between them in life, thereby shutting off the dorsal hiatus. There are several possibilities:

1. Closure by bone originally present. There is no indication in any of the pachyrukhine skulls examined that an independent ossicle was ever

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present in the space occupied by the midcranial hiatus, even though the caudal margin of the preotic flange is probably not entirely complete in any specimen examined. If during life the flange made contact with the ventral section of the hiatal ridge, the result would have been the closing off of a part, but certainly not all, of the hiatus.

In Lepus californicus the elongated caudoventral end of the interparietal projects under the squamosal bar and into the hiatus (fig. 18B), where it freely inserts between the squamosal and petrosal, effectively locking them together. Bramble (1989) called this projection the hiatal plate and interpreted it as another, albeit passive, component of the jackrabbit’s ICJ: because it does not articulate suturally with the petrosal, it “does nothing to impede movement along the intracranial joint” ( Bramble, 1989: 307). In wellpreserved pachyrukhine skulls the shelflike tentorial processes of the supraoccipital and parietal/ interparietal can be seen through the hiatal opening; they do not actually project into the latter, but do form a strong sutural bond with the petrosal crest in the tentorium osseum (figs. 11D, 12C). Rather than having anything to do with the hiatus as such, then, perhaps in both leporids and pachyrukhines the arrangement of these outgrowths acts to reinforce the bony framework of the caudal cranium. This interpretation does not, however, explain the presence or orientation of the organized array of bony edges and spicules that constitutes the dorsal hiatal ridge.

2. Undifferentiated dense connective tissue. Rather than by bone, the midcranial hiatus might have been closed by membrane, continuous with the primitive ectomeninx (cf. MacPhee, 1981). Such tissues cover the midcranial hiatus in leporids as well as the piriform fenestra in shrews and some other eulipotyphlans ( Gasc, 1963; MacPhee, 1981; personal obs.). The appearance and radial disposition of the pachyrukhine dorsal hiatal

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ridge recalls the kind of marginal ectopic ossification that may occur at bony attachment points of dense connective tissues under significant, repeated stress. Muscle attachment to such tissues might produce sufficient stress to initiate the ossification of the latter; this is often a pathological process ( Standring, 2009) but of course need not be (e.g., production of sagittal crest for temporalis m.).

A feature of possible relevance in this regard is the stout projection (thecal spine) on the rostral thecal wall, situated in an exposed position just above the hiatal ridge (figs. 8B–D, 12A) and often damaged or broken in fossils (fig. 9A). The spine is in line with and appears to be functionally related to the linea temporalis for the origin of temporalis m. Alternatively, it may have acted as an attachment for a well-developed pinnal extrinsic such as parietoauricularis m. or its equivalent—an attractive argument if pachyrukhines possessed large, heavy external ears. The spine’s prominence may have been due to the large number of muscle fibers arising from it, perhaps because there was insufficient area for a more rostral attachment. This might have been the case if the hiatus were exclusively covered by membrane.

3. Membranous port for blood vessels. In all notoungulates examined, the medial wall of the theca is deeply incised by the large sulcus for the transverse sinus (fig. 9B, 15B, 17C). This sinus and its various tributaries presumably drained to the jugular/occipital system of veins via several ports, including the posttemporal, jugular, and retroarticular foramina. In pachyrukhines, however, this last aperture is missing as such, because the preotic portion of the cranial wall is largely unossified. Apparently, the retroarticular sinus simply passed through the midcranial hiatus in order to join the jugular system, as suggested by the presence of truncated sulci that suddenly end on the immediately adjacent thecal wall. (Misinterpreting the relevant morphology, Sinclair [1909: 89] stated that he was unable to find a “postglenoid” foramen in Pachyrukhos , as all the skulls he examined displayed a “fracture” in the relevant area.) From one standpoint it could be said that pachyrukhines differed from other notoungulates in possessing a greatly enlarged, membranous retroarticular foramen (which may have carried an artery as well as a vein). However, hiatal width in pachyrukhines is surely much larger than any plausible diameter for transiting blood vessels, indicating that this cannot be the complete explanation for the gap’s presence.

4. Rarefaction zone within the squamosal. Whatever the functional reasons for their appearance, the various fenestrations or rarefactions characteristic of leporid crania are not random in their disposition or patterning ( Wible, 2007; Moss and Feliciano, 1977). This point applies not only to the specific elements affected, but also to features consistently lying within their territories (such as the large dorsal foramen consistently seen in the fenestrated nuchal area of Lepus californicus ; fig. 18B). Fenestration in pachyrukhine cranial bones is more restrained, but it exists (see Sinclair, 1909: pl. X, fig. 1) and is likewise patterned. This raises the question whether the midcranial hiatus could be interpreted as a particularly large and continuous zone of orchestrated bone loss within the territory of the squamosal, without having to infer that its presence was due to the transmission of an outsized vessel. In this argument, absent the hiatus and with normal ossification patterns restored, the pachyrukhine cranial sidewall—including the epitympanic theca—would now be in seamless continuity with other squamosally derived material, just as in other notoungulates in which the hiatal opening is lacking. This explanation is attractive primarily because it solves the morphological paradox of inflating a large epitympanic sinus entirely from within the confines of a tiny bone territory (squamosal bar) situated far from the primordial location of the competent tissue apparently responsible for inducing middle ear expansion (epithelial lining of the developing cavum tympani; see Thompson and Tucker, 2013).

The first three interpretations of the morphological significance of the midcranial hiatus are

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deformation. Pars canalicularis of the petrosal contributes to floor of posttemporal canal, but as it is not exposed externally to any significant extent (see fig. 15D) it is not colored as such in key diagrams. Although entotympanic (ENT?) participation in bulla is considered highly likely, decisive evidence would have to come from early stages (see text). This specimen is well preserved, but it nonetheless exhibits several fractures that superficially mimic sutures. In C, feature a is situated in a location similar to the “sutura squamoso-serrialis” in Roth’s (1903) illustration of a young Toxodon (fig. 2). Another break, nearly the mirror image of this one, occurs in the same position on the right side (not shown). The explanation for their presence may be taphonomic: large vascular channels (transverse sinus and tributaries, situated just beneath the cranial roof in this area) may increase the likelihood of postmortem fracturing (e.g., fig. 14B).

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uncontroversial in the sense that they do not require any unusual developmental processes, whatever their likelihood may be on other grounds. However, they presuppose a very small squamosal component in the theca, perhaps no larger than the area circumscribed by the hiatal ridge (fig. 9B). By contrast, the fourth interpretation asserts that the squamosal was actually of normal size and relations in pachyrukhines, but for unknown reasons developed an extensive rarefaction zone within its caudal portion.

Another taxon that sheds light on the organization of the pachyrukhine caudal cranium is the kangaroo rat Dipodomys , which exhibits hypertrophied paratympanic spaces in combination with a highly reduced squamosal but lacks the

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morphological correlates of the ICJ. Thanks to Webster’s (1975; see also Webster and Webster, 1975) exhaustive studies of ear region ontogeny in this heteromyid, there is no question about the individual contribution of bone territories to the formation of the epitympanicum (= epitympanic sinus/theca of this paper). In the kangaroo rat this volume is exclusively covered by the petrotympanic (both elements participating); the squamous squamosal is reduced to a bar (suprameatal spine of the squamosal; fig. 19A), which is applied against, but not fused to, the dorsal wall of the external acoustic meatus. The parietals, interparietals, and supraoccipital make no contribution to the walls of the epitympanicum ( Beer, 1965).

The demonstrable separateness of the squamosal throughout ontogeny in Dipodomys is a key difference from Paedotherium , in which, as virtual sectioning shows (figs. 10–12), most of the theca is squamosally derived. This observation does not establish that the pachyrukhine hiatus is therefore due to rarefaction in the manner discussed above, but it does allow the presumption that this group differs from other notoungulates only in the degree of definitive squamosal development, and that in no regard is it necessary to invoke the existence of an independent serrialis to explain the origin of the thecal covering.

On this point comparison to heteromyids is again useful, for they likewise vary in the degree of squamosal participation in the cranial sidewall ( Webster and Webster, 1975; Nikolai and Bramble, 1983). In heteromyines (e.g., Liomys ), the squama of the squamosal is still small compared to that of most eutherians, but it is large enough to contribute to the cranial wall dorsal to the meatus. In dipodomyines and also in perognathines ( Perognathus , Chaetodipus ) this portion is always small, never amounting to much more than the tiny rod seen in Dipodomys . Interestingly, this difference is correlated with the scale of paratympanic pneumatization: in heteromyines inflation is relatively conservative, but in some dipodomyines, of which Dipodomys deserti is the outstanding example ( Webster, 1975; Best et al., 1989), pneumatization is so extensive that the combined volume of the two middle ears exceeds that of the braincase.