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Reviewing the Morphology of the Jawclosing Musculature In THE ANATOMICAL RECORD 294:915–928 (2011) Reviewing the Morphology of the Jaw-Closing Musculature in Squirrels, Rats, and Guinea Pigs with Contrast-Enhanced MicroCT PHILIP G. COX* AND NATHAN JEFFERY Department of Musculo-skeletal Biology, University of Liverpool, Sherrington Buildings, Ashton Street, Liverpool, L69 3GE, UK ABSTRACT Rodents are defined by their unique masticatory apparatus and are frequently separated into three nonmonophyletic groups—sciuromorphs, hystricomorphs, and myomorphs—based on the morphology of their mas- ticatory muscles. Despite several comprehensive dissections in previous work, inconsistencies persist as to the exact morphology of the rodent jaw-closing musculature, particularly, the masseter. Here, we review the literature and document for the first time the muscle architecture nonin- vasively and in 3D by using iodine-enhanced microCT. Observations and measurements were recorded with reference to images of three individu- als, each belonging to one of the three muscle morphotypes (squirrel, guinea pig, and rat). Results revealed an enlarged superficial masseter muscle in the guinea pig compared with the rat and squirrel, but a reduced deep masseter (possibly indicating reduced efficiency at the inci- sors). The deep masseter had expanded forward to take an origin on the rostrum and was also separated into anterior and posterior parts in the rat and squirrel. The zygomaticomandibularis muscle was split into ante- rior and posterior parts in all the three specimens by the masseteric nerve, and in the rat and guinea pig had an additional rostral expansion through the infraorbital foramen. The temporalis muscle was found to be considerably larger in the rat, and its separation into anterior and poste- rior parts was only evident in the rat and squirrel. The pterygoid muscles were broadly similar in all three specimens, although the internal ptery- goid was somewhat enlarged in the guinea pig implying greater lateral movement of the mandible during chewing in this species. Anat Rec, 294:915–928, 2011. VC 2011 Wiley-Liss, Inc. Key words: microCT; contrast-enhanced; rodent; masseter; temporalis; pterygoid The masticatory apparatus of rodents is unique among mammals and defines the order Rodentia. As well as Grant sponsor: Natural Environment Research Council possessing an extremely unusual dentition—a pair of (NERC); Grant number: NE/G001952/1. grossly enlarged incisors separated from the cheek teeth *Correspondence to: Philip G. Cox, Department of Musculo- by a large diastema—rodents have a highly distinctive skeletal Biology, University of Liverpool, Sherrington Buildings, arrangement of masticatory muscles. The masseter is by Ashton Street, Liverpool, L69 3GE, UK. Fax: þ44 151 794 5517. far the dominant jaw-closing muscle in the Rodentia, E-mail: [email protected] comprising between 60% and 80% of the entire mastica- Received 10 February 2011; Accepted 17 February 2011 tory muscle mass (Turnbull, 1970). Furthermore, the DOI 10.1002/ar.21381 musculature has become specialized to accomplish not Published online 28 April 2011 in Wiley Online Library only gnawing at the incisors and chewing at the molars (wileyonlinelibrary.com). VC 2011 WILEY-LISS, INC. 916 COX AND JEFFERY but also propalinal movement of the lower jaw between dea (pocket gophers, kangaroo rats, and mice). In the these two feeding modes (Becht, 1953). These movements hystricomorph masticatory apparatus, a deeper part of are necessary in rodents, because it is impossible for the the masseter has extended forward, through the orbit incisors and cheek teeth to be in occlusion at the same and the grossly enlarged infraorbital foramen to take an time, and thus, incision and mastication have become origin on the snout. This morphology is found in the mutually exclusive activities (Hiiemae and Ardran, 1968). Caviomorpha (South American rodents), Phiomorpha Given the unique demands on the masticatory apparatus, (African mole-rats, cane rats, and the dassie rat) and it is perhaps unsurprising that the morphology of the Hystricidae (old world porcupines) as well as the previ- jaw-closing muscles, in particular the masseter, has long ously mentioned Pedetidae, Anomaluridae, Dipodidae, been used to classify the rodents into subgroups. and Ctenodactylidae. Finally, the myomorphs combine Brandt (1855) first used features primarily from the sciuromorph and hystricomorph features with the ori- masticatory apparatus to group rodents into squirrel- gins of both parts of the masseter having migrated on to like (Sciuromorpha), mouse-like (Myomorpha), and por- the rostrum. This condition is seen in the Muroidea cupine-like (Hystricomorpha) forms (Brandt’s fourth (mice and rats) and the Gliridae (dormice). group Lagomorpha, the rabbits, hares, and pikas, now The above morphological descriptions have been occupy a separate, albeit closely related, order). These greatly complicated by the complete lack of consensus on three suborders were largely retained with only minor the nomenclature of rodent masticatory muscles, with revisions by most workers for the next century (e.g., particular regard to the masseter (hence the lack of spe- Thomas, 1896; Miller and Gidley, 1918) and indeed were cific muscle nomenclature in the previous paragraph). still the basis for rodent taxonomy in George Gaylord Part of the confusion arises due to the uncertainty of Simpson’s monumental classification of the mammals in how many layers the masseter divides into, and whether 1945. It should be noted, however, that Simpson alluded all of these layers should be referred to as the masseter to a growing dissatisfaction with the three suborders or as entirely separate muscles. This uncertainty per- (Simpson, 1945, p.198) but retained them in his work sists despite several thorough descriptive articles based owing to a lack of a better alternative at that time. The on gross dissection (in particular, compare Hiiemae and problem with the three suborder arrangement can be Houston, 1971 with Weijs, 1973; see also Turnbull, 1970; clearly seen in Simpson’s classification: there are a num- Woods, 1972; Cooper and Schiller 1975; Ball and Roth, ber of rodent families that do not neatly fit into the 1995; Druzinsky, 2010a). A possible cause of much of Sciuromorpha, Myomorpha, or Hystricomorpha. In par- this uncertainty is methodological in that information on ticular, the Anomaluridae (scaly-tailed squirrels), Pedeti- muscle morphology is typically gathered invasively by dae (springhare), Dipodidae (jerboas, jumping mice, and dissection, and thus, superficial structures are destroyed birchmice), Bathyergidae (mole-rats), and Ctenodactyli- in gaining access to the deeper structures and spatial dae (gundis) have all posed problems to various workers relationships are difficult to define accurately. On the in the past. A competing classification of rodents, first basis of the work by Metscher (2009), Jeffery et al. proposed by Tullberg (1899), split the Rodentia into two (2011) recently developed an alternative, nondestructive suborders (Sciurognathi and Hystricognathi) based on approach that has the potential to reveal detailed infor- the morphology of the angular process of the mandible. mation on rodent masticatory muscle morphology in This system overlaps with the masseter-based classifica- situ. In this method, the biological specimen is soaked in tion in some respects, such as the fact that all hys- a solution of iodine for a number of weeks before scan- tricognaths have a hystricomorph muscle arrangement ning, which allows the detailed imaging of soft tissues (Lavocat, 1974; Wood, 1974), but has notable differences and hard tissues. Here, we use this novel technique in as well, particularly that sciurognaths can possess any reviewing the structure, arrangement, and terminology of the three masticatory muscle morphologies (Offer- of the masticatory apparatus in three rodents displaying mans and De Vree, 1989). the sciuromorph, hystricomorph, and myomorph muscle Neither of the two classifications outlined above has arrangements. Descriptions of the masticatory muscles stood the test of time. Although evidence points toward will be reported, comparisons with previous work will be a monophyletic Hystricognathi, the Sciurognathi is made, and current controversies will be addressed. almost certainly a paraphyletic grouping, and the idea Given the importance of rodents and knowledge of their that the three suborders of Brandt (1855) and Simpson musculature to many scientific disciplines other than (1945) represent monophyletic groups of rodents is now anatomy, in particular evolutionary developmental biol- generally discredited (Adkins et al., 2001; Huchon et al., ogy (Hallgrı´msson et al., 2007; Jones et al., 2007; Hall- 2002; Adkins et al., 2003; Blanga-Kanfi et al., 2009). grı´msson and Lieberman, 2008; Parsons et al., 2008), it However, the use of the terms sciuromorph, myomorph, is felt that such a review is timely and necessary. and hystricomorph as adjectives describing particular arrangements of jaw-closing muscles has persisted, MATERIALS AND METHODS largely thanks to Wood (1965). In his work, Wood Sample describes the primitive arrangement of rodent mastica- tory muscles (the ‘‘protrogomorph’’ condition, found in Three rodent species were chosen that possess the most pre-Oligocene fossil rodents and also in the extant sciuromorph, hystricomorph, and myomorph morpholo- mountain beaver, (Aplodontia rufa), and the three gies. These were, respectively, the Eastern grey squirrel arrangements derived from it.
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