AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 112:517–540 (2000)

Why Fuse the Mandibular Symphysis? A Comparative Analysis

D.E. LIEBERMAN1,2 AND A.W. CROMPTON2 1Department of Anthropology, George Washington University, Washington, DC 20052, and Human Origins Program, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560 2Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138 KEY WORDS symphysis; mammals; primates; electromyograms; mandible; mastication

ABSTRACT Fused symphyses, which evolved independently in several mammalian taxa, including anthropoids, are stiffer and stronger than un- fused symphyses. This paper tests the hypothesis that orientations of tooth movements during occlusion are the primary basis for variations in symph- yseal fusion. Mammals whose teeth have primarily dorsally oriented occlusal trajectories and/or rotate their mandibles during occlusion will not benefit from symphyseal fusion because it prevents independent mandibular move- ments and because unfused symphyses transfer dorsally oriented forces with equal efficiency; mammals with predominantly transverse power strokes are predicted to benefit from symphyseal fusion or greatly restricted mediolateral movement at the symphysis in order to increase force transfer efficiency across the symphysis in the transverse plane. These hypotheses are tested with comparative data on symphyseal and occlusal morphology in several mammals, and with kinematic and EMG analyses of mastication in opossums (Didelphis virginiana) and goats (Capra hircus) that are compared with published data on chewing in primates. Among mammals, symphyseal fusion or a morphology that greatly restricts movement correlates significantly with occlusal orientation: species with more transversely oriented occlusal planes tend to have fused symphyses. The ratio of working- to balancing-side ad- ductor muscle force in goats and opossums is close to 1:1, as in macaques, but goats and opossums have mandibles that rotate independently during occlu- sion, and have predominantly vertically oriented tooth movements during the power stroke. Symphyseal fusion is therefore most likely an adaptation for increasing the efficiency of transfer of transversely oriented occlusal forces in mammals whose mandibles do not rotate independently during the power stroke. Am J Phys Anthropol 112:517–540, 2000. © 2000 Wiley-Liss, Inc.

During early development, all mammals edentates (e.g., Bradypodidae), and many have a chondrogenic, fibrocartilagenous artiodactyls (Camelidae, Hippopotamidae, symphysis between the two mandibles in Suidae, and Tayassuidae), the symphysis which lateral growth occurs (de Beer, 1937; Moore, 1981; Enlow, 1990). The mandibular Grant sponsor: National Science Foundation; Grant number: symphysis remains unfused throughout life IBN 96-03833. in most mammalian species, but in several *Correspondence to: Daniel E. Lieberman, Department of An- thropology, George Washington University, 2110 G St. NW, taxa, including anthropoid primates, most Washington, DC 20052. E-mail: [email protected] perissodactyls, hyracoids, vombatidae, some Received 19 May 1998; accepted 22 November 1999.

© 2000 WILEY-LISS, INC. 518 D.E. LIEBERMAN AND A.W. CROMPTON fuses prior to or roughly at the time that caque (Macaca fascicularis) but is about occlusion commences. In addition, partial- 3.5:1 in the thick-tailed bushbaby galago to-complete fusion occurs late in postnatal (Otolemur crassicaudatus). Given the high development in some species in which juve- correlation between adductor muscle con- niles typically have unfused symphyses tractile activity and strain magnitudes, Hy- (Beecher, 1977a; Scapino, 1965, 1981; Ra- lander (1986, 1979a,b) and Ravosa and Hy- vosa and Simons, 1994). lander (1993, 1994) interpreted the W/B There is general agreement that the prin- strain ratios that approach 1:1 in the ma- cipal advantage of an unfused mandibular caque as evidence for the recruitment of symphysis is to allow independent or semi- more dorsally oriented force from the bal- independent movement of the two mandi- ancing-side adductor muscles to generate bles during occlusion (Kallen and Gans, occlusal force on the working side during 1972; Hylander, 1979b; Scapino, 1981). unilateral mastication and biting. Ravosa There is less consensus, however, about why and Hylander (1993, 1994) therefore sug- mandibular fusion evolved convergently in gested that a fused symphysis may be an certain taxa. Two general types of argu- adaptation to prevent structural failure ments have been proposed. The most com- from the repeated high magnitudes of strain mon is that symphyseal fusion is an adap- that these transferred forces generate. tation to strengthen the mandible in the A second, complementary hypothesis is symphyseal region. Strength, defined here that symphyseal fusion is an adaptation to as the ability to resist structural failure in stiffen the mandible in the symphyseal re- response to applied forces, is an important gion. Stiffness, defined here as the ability to adaptation in bone tissue that helps to resist deformation in response to applied maintain structural integrity so that a bone forces,1 is the primary mechanical property can remain stiff (Currey, 1984; see below). of bones which enables them to transfer Arguments about the adaptive basis for force (Currey, 1984, p. 3–4). Several types of symphyseal strength have been proposed arguments have been made that the fused primarily for primates. DuBrul and Sicher symphysis evolved as an adaptation for (1954) and Tattersall (1973, 1974) sug- stiffness. In the case of primates, Kay and gested that fusion was an adaptation in Hiiemae (1974a,b) and more recently higher primates to resist large medial and Greaves (1988, 1993) suggested that symph- lateral transverse bending forces caused by yseal fusion stiffens the symphysis during adductor muscles. Beecher (1977a,b, 1979), incisal biting of hard objects, thereby pre- noting partial fusion of the symphysis in venting any potentially inefficient dissipa- many prosimians, proposed that the fused tion of dorsally-directed force across the symphysis in higher primates helps to resist symphysis. Ravosa and Hylander (1993, elevated magnitudes of dorso-ventral shear 1994), however, rejected this hypothesis by generated by larger bite forces associated noting that primates with fused symphyses with anthropoid primate diets. Analyses of rarely if ever use their incisors to crush in vivo strain and muscle function (Hy- hard objects. In a more general argument lander, 1977, 1979a, 1984, 1986; Hylander based on a comparative analysis of the and Johnson, 1985, 1994; Hylander et al., structure of unfused symphyses in car- 1987, 1992) demonstrated that during mas- nivorans, Scapino (1981) suggested that tication, anthropoid primates not only gen- symphyseal fusion is an adaptation for erate high magnitudes of twisting strain transferring proportionately higher occlusal and lateral transverse bending (known as forces from the balancing- to working-side “wishboning”) during the power stroke, but mandibular corpora. According to this hy- also experience similar strain magnitudes on the balancing-side and working-side mandibular corpora. According to Hylander 1Note that strength and stiffness are different properties. Many stiff substances such as glass have little strength because (1979a), the ratio of working-side to balanc- they are brittle, and relatively elastic tissues such as muscle or ing-side strain (W/B) in the mandible is ap- tendon are strong because they are not stiff. In addition, strength and stiffness are planar. Tendon is strongest along its proximately 1.5:1 in the crab-eating ma- long axis, the plane in which it has some elasticity. WHY FUSE THE MANDIBULAR SYMPHYSIS? 519 pothesis, mammals with unfused symphy- evidence that fusion is correlated with a ses generate proportionately lower forces stronger mandibular symphysis in higher when they chew than mammals with fused primates, it is not evident that fusion per se symphyses. However, Dessem (1985) is a means of strengthening rather than showed that fused and unfused symphyses stiffening the symphysis. Given the essen- transfer dorsally oriented forces with equal tial adaptation of bone tissue is to be stiff, it efficiency2 from the balancing to working follows that bones require strength primar- sides. In mammals with unfused symphy- ily in those planes in which they resist de- ses, rapid and complete force transfer occurs formation (Wainright et al., 1976; Currey, because cruciate ligaments and/or interdig- 1984). As noted above, both unfused and itating rugosities (see below) create suffi- fused symphyses efficiently transfer force in cient stiffness in the sagittal plane to resist the sagittal plane because they remain stiff dorso-ventral shearing movements between in this plane. As a result, both types of sym- the two mandibles. physes must counteract high strains in the sagittal plane solely by adding mass in the AN ALTERNATIVE HYPOTHESIS same plane. This principle may explain ON THE ADAPTIVE BASIS why, with the important exception of pros- OF SYMPHYSEAL FUSION imian primates and some carnivorans This paper tests an alternative hypothe- (Scapino, 1981; Ravosa, 1991, 1996; Ravosa sis (see also Hylander et al., 2000) related to and Hylander, 1994), there is no apparent the idea that symphyseal fusion is an adap- relationship between mandibular size and tation to stiffen the mandible. We propose symphyseal fusion in most mammalian that the orientations of the movements of taxa. Because of the negative allometry be- the lower teeth relative to the upper teeth tween cranial size and jaw muscle size, during occlusion are the primary basis for larger mammals have proportionately variations in symphyseal fusion.3 Although smaller cross-sectional areas of their adduc- unfused symphyses appear to be as effective tor muscles, and therefore might be ex- as fused symphyses in transferring dorsally pected to recruit more balancing-side mus- oriented force (see above), the fused sym- cle force to generate equivalent working- physis, by virtue of its stiffness in all planes, side bite forces (Ravosa, 1991, 1996). is likely to be more effective transferring Symphyseal fusion, however, does not ap- force in the transverse plane. As a result, it pear to be correlated with body-size varia- is predicted that mammals with a strong tion within nonprimate mammal and some transverse component of intercuspal move- carnivoran lineages. For example, all Bovi- ment during occlusion will benefit from a dae, from dik-diks to water buffalo, have fused symphysis or from other adaptations unfused symphyses, whereas the paenungu- that restrict medio-lateral movement in the lata, from small hyraxes to large elephants, symphysis. However, mammals whose teeth have fused symphyses. Thus, while the high require some degree of rotation during oc- W/B strain ratios in galagos with unfused clusion and/or who have primarily dorsally symphyses suggest that they recruit less oriented occlusal trajectories will not benefit balancing-side force than macaques with from symphyseal fusion and are predicted to fused symphyses (Hylander, 1979a), this retain an unfused symphysis. pattern may not be generally characteristic Several observations underlie this hy- for other mammals with unfused symphyses pothesis. First, although there is compelling (Crompton, 1995; see below). A second observation is that force transfer is a function of stiffness. The anatomy of the 2The term efficiency here is used in this paper in the context of cruciate ligaments and rugosities of the the timing and degree of force transfer. Stiffness increases the efficiency of force transfer between two objects because no force symphysis stiffen the unfused symphysis in is stored elastically, or dissipated through movement or the the sagittal plane in order to transfer dor- generation of heat. 3We assume here that the movements of the lower and upper sally oriented force efficiently and also to teeth relative to each other during the power stroke reflect to resist antero-posterior forces (Scapino, some extent the orientation of intercuspal force that is gener- ated. 1981), but these structures clearly allow 520 D.E. LIEBERMAN AND A.W. CROMPTON some degree of independent movement of on the degree to which the ligaments are the two mandibles in terms of lateral trans- oriented transversely. verse bending and twisting (Oron and A final indication of the importance of Crompton, 1985). These independent move- transversely directed forces for symphyseal ments can occur because the symphyseal fusion is provided by the experimental stud- ligaments (which are stiff only along their ies by Hylander and Crompton (1986) and long axis) are predominantly oriented verti- Hylander and Johnson (1994) of the rela- cally and obliquely (Beecher, 1977a; tionship between jaw adductor muscle force, 4 Scapino, 1981; see below). If the two man- mandibular movements, and mandibular dibles can twist and wishbone indepen- strain in macaques. Hylander and Cromp- dently to some extent in an unfused sym- ton (1986) and Hylander and Johnson physis, then such movements must (1994) showed that lateral transverse move- generate less strain in the symphyseal mar- ment during the power stroke in macaques gins of an unfused than a fused symphysis. occurs because maximum contraction of the These strains presumably dissipate in the working-side (W) medial pterygoid and the ligaments that connect the symphyses, just balancing-side (B) deep masseter occur sig- as Herring and Mucci (1991) showed to oc- nificantly later (by 26 msec on average) than cur in the zygomatic suture. In other words, the balancing-side medial pterygoid and the fused symphyses are predicted to lay down working-side deep masseter. The former bone in order to resist high twisting and muscles not only adduct but also pull the wishboning strains because they are stiff in mandible medially, and these transverse all planes, whereas unfused symphyses of movements correlate strongly with peak noncarnivoran mammals are predicted to experience high strains primarily from wishboning strains in the symphysis. In ad- dorso-ventral shearing because they are dition, Hylander et al. (1992) demonstrated stiff in just the sagittal plane. It follows that that as macaques chew harder food, they a likely explanation for symphyseal fusion tend to (but do not always) recruit more in most taxa is to increase the efficiency of balancing-side masseter force (approaching force transfer in the transverse plane in or- 1:1 ratios), generating significantly higher der to generate high forces in this plane wishboning strains in the symphyseal re- during occlusion. Because fusion is probably gion. These data, therefore, indicate that the most effective means of stiffening the wishboning in the macaque is primarily a symphysis in the transverse plane, fused function of the recruitment of high levels of symphyses may require additional mass in balancing-side muscle force whose primary the transverse plane in order to counteract function is to pull the mandible medially. In high wishboning and twisting strains that other words, mammals in which more me- would result from any stiffness that fusion dial movement of the teeth of the working creates (Hylander, 1988; Hylander et al., side occurs during the power stroke are pre- 1987; Hylander and Johnson, 1994; Ravosa dicted to transfer proportionately more and Hylander, 1994). As noted above, un- transversely oriented balancing-side muscle fused symphyses can vary in their degree of force across the symphysis. Therefore, wish- stiffness in the transverse plane, depending boning strains within the mandible on ei- ther side of the ligamentous region of the symphysis are predicted to be lower than in 4The structure and loading of the mandibular symphysis in forms with a fused symphysis because of carnivorans is very complex and this group will not be discussed in this paper. It should, however, be pointed out that the symph- more rapid and complete force transfer in sis of this group vary from unfused to interdigitating rugosities the transverse plane. to complete fusion. The carnivoran symphysis is designed not only to transmit forces with varying directions from the balanc- ing- to working-side, but also to resist the high forces generated Hypotheses to be tested by bilateral or unilateral canine use. In the dog, for example, the cruciate ligaments between the central parts of the symphyseal plates have a predominantly antero-posterior orientation, al- Comparative morphological and kine- though there are some transversely and obliquely oriented liga- matic data are used to test four general ments (Scapino, 1981). This arrangement suggests that resisting antero-posteriorly directed forces is important. hypotheses predicted by the above model. WHY FUSE THE MANDIBULAR SYMPHYSIS? 521 Hypothesis 1. Mammal species (with the temporalis) as well as combined ratios for exception of carnivorans) with a strong just the superficial and deep masseters. We transverse component of intercuspal move- focus on the masseter ratios, in part, be- ment during the power stroke are predicted cause the study by Hylander et al. (1987) of to have fused symphyses. Because the ori- W/B ratios in the macaque measured just entation of wear facets reflects the direction the deep and superficial masseters. If this of tooth and jaw movements during occlu- specific hypothesis is not rejected, then the sion (e.g., Smith and Savage, 1959; Mills, more general hypothesis that symphyseal 1967; Crompton and Kielan-Jaworowska, fusion is an adaptation to strengthen the 1978; Janis, 1979b; Oron and Crompton, mandible in response to proportionately 1985), this hypothesis can be tested by com- higher forces that transfer across symphysis paring symphyseal morphology with mea- may not be true of all mammals, but instead surements of the orientation of the occlusal may be a specific explanation for the evolu- wear facets of the molars relative to the tion of symphyseal fusion in primates. transverse plane. In particular, the hypoth- esis predicts a significantly more transverse Hypothesis 3. Mammals with unfused orientation of some of the upper and lower symphyses are predicted to have some de- molar wear facets in mammals with fused gree of independent rotation (inversion and rather than unfused symphyses, tested eversion) of the mandibles, presumably to against the null hypothesis that there is no match the steep occlusal planes of occluding significant difference between these groups. teeth (Oron and Crompton, 1985). The study by Oron and Crompton (1985) of the tenrec, Hypothesis 2. Since the unfused symphy- which has a highly mobile symphysis, dem- sis transfers dorsally oriented forces effec- onstrated that the ventral margin of the tively (Dessem, 1985), the pattern docu- mandible inverts prior to the power stroke mented by Hylander (1979a) for galagos, in and then everts during the power stroke, which the W/B ratio of mandibular strain thereby moving the lower trigonid in a dor- was roughly 3.5:1, is not predicted to be sal and lingual direction during occlusion characteristic of other mammalian taxa into and out of the embrasure between the with unfused symphyses. This study, how- upper trigons. The marked rotation ob- ever, uses electromyogram (EMG) data rather than mandibular strain data to ex- served in the tenrec is associated with the amine directly the ratio of W/B force in the virtual absence of a deep masseter that sta- jaw adductor muscles, because EMG poten- bilizes the mandible. A similar though less tials provide a more direct test of the hy- marked degree of rotation is expected in the pothesis that mammals with fused symphy- goat and the opossum, both of which have ses recruit more balancing-side force than well-developed deep masseters. In addition, mammals with unfused symphyses. An- the pattern of medial pterygoid activity is other reason to focus on EMG data is that expected to differ in mammals with unfused strain magnitudes have the potential to re- symphyses whose mandibles rotate around flect aspects of masticatory kinematics and their long axes during unilateral mastica- mandibular corpus shape that do not corre- tion. The medial pterygoid is the only major late directly with muscle force recruitment adductor which causes the ventral margin (Daegling, 1993). Therefore, the specific hy- of the mandible to invert, counteracting the pothesis to be tested here is that the ratio of everting tendency of the masseter. There- W/B muscle force generated in mammals fore, these muscles are predicted to have with unfused symphyses while chewing different patterns of activity in mammals hard or resistant food should be roughly with fused and unfused symphyses. The me- comparable to that of mammals with fused dial pterygoid is predicted to contract bipha- symphyses (i.e., close to 1:1). In particular, sically in the goat and the opossum, pre- we examine combined activity levels of all sumably to invert the mandible prior to the major jaw adductors (deep masseter, su- occlusion, and then to help control the ten- perficial masseter, medial pterygoid, and dency of the masseter and temporalis mus- 522 D.E. LIEBERMAN AND A.W. CROMPTON cles to evert the mandible during the power details, see Crompton and Hiiemae, 1970; stroke. Crompton and Kielan-Jaworowska, 1978; Hiiemae and Crompton, 1985). Molars of Hypothesis 4. Finally, the above-de- this type are characterized by embrasure scribed hypotheses concerning differences shearing in which the tall trigonid of the in masticatory kinematics are predicted to lower molar fits precisely and tightly into a correlate with differences in the cross-sec- V-shaped embrasure between two upper tional morphology of the symphysis between molars. Shearing takes place between the species with fused and unfused symphyses. leading edges of the crests connecting the In contrast to the fused symphysis in spe- main cusps. The occlusal angle is steep, and cies such as the crab-eating macaque which little transverse movement occurs during is stiff in all planes, the structure of the occlusion: dorsally oriented jaw movement unfused symphysis is predicted to ensure (about 80° relative to the transverse plane stiffness in the sagittal plane but to allow of the tooth row) stops when the protocone some degree of independent movement in fits into the talonid basin; movement of the other planes. lower molars out of occlusion is directed al- most entirely ventrally, although with a Hypothesis testing slight degree of mandibular rotation (Cromp- To test hypothesis 1, we compare the ori- ton and Hiiemae, 1970; see also below). entation of occlusal wear facets in a compar- In goats, the molars are also designed to ative sample of herbivorous mammals with shear food, but in contrast to mammals with fused and unfused symphyses. Hypotheses a tribosphenic molar, shearing surfaces in 2–4 are tested with data on symphyseal the goat are aligned parallel to the longitu- morphology, and on the kinematics and dinal axis of the tooth row; shearing in- EMG patterns of muscle activity during volves extensive movement of the lower jaw mastication in the goat (Capra hircus) and in a medial direction. Artiodactyl molars are the American opossum (Didelphis virgini- selenodont, with two sets of “selenes” or ana), which we compare with previously half-moon-shaped lophs, each with a labial published data on these aspects of mastica- and lingual loph (Janis, 1979a). Food is sub- tion in the macaque (Macaca fascicularis) jected to a “double chop” as the antero-pos- from Crompton and Hylander (1986), Hy- teriorly aligned lophs of the lower molars lander and Crompton (1986), and Hylander are drawn across those of the uppers at an et al. (1987, 1992). angle of approximately 45–50° relative to As a caveat, we stress that hypotheses the horizontal plane. Occlusion is therefore 2–4 are tested here with only a small num- characterized by a single stroke that com- ber of taxa. Integrated kinematic, EMG, bines both vertical and transverse move- and histological data are needed on more ment (de Vree and Gans, 1976). taxa with fused and unfused symphyses to In macaques, as in most anthropoids, the determine the extent to which galagos are lower molars initially move into occlusion at representative of prosimians, macaques are a steep angle. However, the power stroke in representative of mammals with fused sym- anthropoids, including humans, tends to be physes, and goats and opossums are repre- predominantly transverse, typically within sentative of mammals with unfused sym- 30° of the horizontal plane (Kay and Hii- physes. However, the differences between emae, 1974b; Proschel, 1987; Wong, 1989; opossums, goats, and macaques in terms of Miller, 1991). In contrast to tribosphenic symphyseal structure and occlusal kinemat- molars, the crushing surfaces of opposing ics make them especially useful for an ini- molars are relatively larger. Crushing oc- tial attempt to test hypotheses about the curs between the hypocone and protocone of relationship between symphyseal fusion the upper molars and the trigonid basin and and chewing. Mammals such as the opos- talonid of the lower molars. Although it was sum and several insectivores possess tribos- originally believed that the primate power phenic molars, and thus have a very gener- stroke was divided into distinct dorsal alized, primitive pattern of occlusion (for (phase I) and lingual (phase II) components WHY FUSE THE MANDIBULAR SYMPHYSIS? 523 (Kay and Hiiemae, 1974a,b), it is now evi- the same individual indicate that these dent that there is no clear distinction be- wear facet angles are accurate to within a tween these phases, and that the power few degrees. stroke occurs during predominantly trans- A Mann-Whitney U-test was used to test versely oriented movements of the lower if upper and lower wear facet angles are teeth relative to the upper teeth (Hylander more horizontal in species with fused than et al., 1987; Hylander and Johnson, 1994). unfused symphyses against the null hypoth- Phase II, if it exists, occurs as occlusal forces eses that they do not differ significantly. decline (Hylander et al., 1987). Comparative symphyseal morphology MATERIALS AND METHODS The histology and structure of the man- dibular symphysis were examined in speci- Comparative occlusal morphology mens of the three species for which we To test the hypothesis that mammals present experimental data: C. hircus, M. with fused symphyses tend to have a more fascicularis, and D. virginiana. Mandibles transversely oriented component of move- of adult C. hircus and D. virginiana were ment during the power stroke than those defleshed, fixed in formaldehyde, cleared with unfused symphyses, the orientation of with xylene, dehydrated in ethanol, and the occlusal planes of the upper and lower then embedded in Osteobed™. A mandible second permanent molars was measured of a juvenile macaque (permanent incisors relative to the plane of the tooth row on and canines had not yet erupted) was em- pooled-sex samples of 4 adult skulls from 12 bedded in Castrolite™. Serial ground sec- diverse species of herbivorous mammals tions were cut in the coronal plane (trans- from the Museum of Comparative Zoology verse to the longitudinal axis) of the jaw at (Harvard University). These mammals were 1-mm intervals with an Isomet™ diamond chosen because they sample a wide range of saw, mounted to glass slides with Epotek™ sizes and families. Mammals with fused 310 epoxy, and ground and polished to a symphyses include Camelus dromedarius, thickness of approximately 100 ␮m. Sec- Rhinocerus unicornis, Equus caballus, Lama tions were examined in plain and cross-po- huanachus, Macaca fascicularis, Procavia larized transmitted light, and photographed capensis, and Sus scrofa. Mammals with un- with Kodak Ektachrome™ slide film fused symphyses include Didelphis virgini- (Kodak, Rochester, NY). The resultant color ana, Capra hircus, Cervus elaphus, Gazella slide was scanned with a Polaroid Sprint- gazella, Lemur fulvus, and Odocoileus vir- Scan35 connected to a Power Macintosh giniana. In all species, we measured the 8500/120 and printed on a Tektronix Phaser angle formed by the apices of the entoconid 560. and hypoconid wear facets of the M and the 2 Experimental subjects angle formed by the apices of the metacone and hypocone wear facets of the M2 relative We report the results of experiments in to the transverse plane of the tooth row. The opossums (Didelphis virginiana) and goats transverse plane of the tooth row was deter- (Capra hircus; breed: Nubian). Three opos- mined by placing an index card across the sums adults (O1, O2, and O3) were recorded deepest point of the left and right second while masticating different foods during molars. Wear facet angles in all species each experiment. We report here the results were measured by affixing a thin rod of when O1 was fed cooked beef, O2 was fed graphite (0.5-mm diameter) with cyanoacry- bone, and O3 was fed both apple and bone. late glue to each wear facet under a dissect- Raw EMGs for O2 when it was chewing ing microscope. The angle of the graphite chicken flesh were published by Crompton rod relative to the transverse plane was re- and Hylander (1986). The two goats (G1, corded on an index card (see above) and G2) were both Nubian goats: G1 was an measured with a protractor accurate to 1°. 18-month-old female adult; G2 was a Following this procedure, the glue was re- 4-month-old male. In all experiments, the moved with acetone. Repeated measures on goats were fed dry hay. 524 D.E. LIEBERMAN AND A.W. CROMPTON EMG electrodes and recording pterygoids. In G2, electrodes were inserted procedure into the left and right deep masseters, su- Opossums. Simultaneous electromyo- perficial masseters, and medial pterygoids. graphic (EMG) measurements of jaw adduc- EMG potentials were amplified between tor activity were recorded in O1–O3 using 2,000–10,000 times, with a low-frequency bipolar fine-wire electrodes inserted into cutoff at 300 Hz, filtered at 60 Hz, and re- left and right sides of the following muscles. corded on a TEAC RD 145T DAT recorder To place the electrodes, each animal was (TEAC America, Inc., Montebello, CA). Re- anaesthetized using halothane. Electrodes cordings of chewing sequences for each ex- were made from 0.002-inch coated steel wire periment were made over 2 days following (J. Wilbur and Driver Co., Newark, NJ) and surgical implantation of electrodes. After inserted into the muscles using a hypoder- each experiment, still radiographs were mic needle (for protocol, see Gans, 1992). taken to verify electrode position. EMG potentials were amplified between 2,000–10,000 times, with a low-frequency Cineradiographic recording cutoff at 300 Hz, filtered at 60 Hz, and re- In order to correlate EMG activity with corded on a Bell and Howell (Pasadena, CA) jaw movement and to determine balancing CPR 4010™ magnetic tape recorder at 15 and working sides, the animals were filmed inches/sec. In O1, electrodes were inserted in several projections using normal light into the posterior and anterior compart- and X-rays. There were some differences be- ments of the temporalis, the deep masseter, tween experiments in terms of the projec- the superficial masseter, the medial ptery- tions used because of differences in the ex- goid, and the digastric. In O2, electrodes perimental setup and whether strain-gauge were inserted into the posterior, middle, data (not reported here) were also being ac- and anterior compartments of the tempora- quired. lis, the deep masseter, and the superficial masseter. In O3, electrodes were inserted Opossums. Radiopaque metallic fillings into the deep masseter, the superficial mas- were placed in the upper and lower canines seter, and the medial pterygoid. Recordings and third molars of all animals. O1 and O3 of chewing sequences for each animal were were filmed synchronously in frontal view made over 3 days following surgical implan- with a Photosonics 16-mm 1PL camera and tation of electrodes. Verification of electrode in lateral view with an Eclair GV-16 camera placement was made by manual dissection attached to a Siemens image intensifier (ex- after the animals were euthanized with an posure 65 kV, 120 mA). All filming during intracardial injection of sodium pentobarbi- mastication was recorded at 100 frames/sec tol. with Kodak 16-mm Plus-X reversal film (no. 7276). O2 was filmed with the above cinera- Goats. Electrodes were made from 0.004- diographic equipment in both dorso-ventral inch coated silver wire (California Fine Wire and lateral view at 100 frames/sec. Voltage Co., Grover Beach, CA). Electrodes were in- pulses triggered by the camera shutters serted during an asceptic surgical procedure were recorded by the tape recorder, allowing in which strain gauges were also attached to precise synchronization of frames from the the mandibles (the strain data are not re- two sets of the film with the EMG data. ported here). A surgical plane of anesthesia was induced by ketamine (20.0 mg/kg) and Goats. G1 and G2 were both filmed in atropine (0.04 mg/kg) and maintained with dorso-ventral projection at 100 frames/sec halothane (Muir and Hubbell, 1989). A sin- using a GV 16 Photosonics cine camera at- gle incision was made between the ventral tached to a Siemens image intensifier (ex- margins of the two mandibles. In G1, elec- posure 65 kV, 120 mA). Radiopaque metallic trodes were inserted using a hypodermic fillings were placed in the lower first and needle into the left and right deep masse- fourth incisors in G1. G2 was also filmed in ters, superficial masseters, anterior com- lateral projection with Kodak 16-mm Plus-X partments of the temporalis, and medial reversal film (no. 7276). Voltage pulses trig- WHY FUSE THE MANDIBULAR SYMPHYSIS? 525 gered by the camera shutter were recorded tween the lateral edge of the ventral surface on the tape recorder. of the mandible below the ascending process and the medial surface of the dorsal margin Kinematic analysis of the ascending process. The latter lies me- Movements of the mandibles relative to dial to the former; consequently, a decrease each other and to the maxilla (gape, trans- in this distance indicates inversion of the verse movement, and rotation) were mea- ventral margin of the mandible. This tech- sured from the X-ray film. The film was nique cannot be used in the goat because the projected on a Vanguard Motion Analyzer ventral margin of the ramus is not always (Model M160W, Vanguard Instrument visible in dorso-ventral view. Instead, the Corp.) so that selected points could be digi- apparent rotation of the goat symphysis tized with a Graph/Pen Sonic Digitizer around the mandibular axis was estimated (Model C-P-6/50, Science Accessories Corpo- in G1 by measuring the differences in the ration). Kinematic data were recorded only transverse movement of I1 and I4 relative to from sequences in which there was minimal the mid-sagittal plane. Estimating rotation head movement during the chewing cycle is possible because, in dorso-ventral projec- and in which the subject’s head was neither tion, the horizontal distance between I1 and tilted nor flexed. A BASIC software program I4 will decrease when the ventral margin of developed by J. McGarrick (St. Thomas’ the mandible either inverts or everts (see Hospital, United Medical Schools, London, Fig. 7); if no rotation occurs, this distance

UK) was used to calculate the position of remains constant. The distance between I1 marker points relative to the projected trans- and I4 decreases during rotation because verse (X) and mid-sagittal (Y) planes. The the center of rotation of the symphysis, the transverse plane is defined here as the plane fibrocartilagenous pad (see below), lies close of occlusion of the postcanine teeth. Gape was to I1 when the ventral margin of the man- measured directly (as the distance from the dible inverts or everts, so I4 tends to move upper central to lower central incisors) in more medially than I1 when the whole jaw films taken in lateral view; in dorso-ventral shifts medially and everts, and I4 tends to films, gape was estimated by measuring the move more laterally than I1 when the whole relative change in distance between the front jaw shifts laterally and inverts. of the symphysis and the back of the palate as EMG analysis seen in dorso-ventral view. This distance de- creases as the jaw opens and increases as the Selected portions of the EMG data for jaw closes, but it only approximates gape, which kinematic sequences were also avail- since head movements during feeding can able (see above) were played through an also affect this projected distance. As mea- A-D converter into a Macintosh computer at sured here, presumptive gape tends to be a 10,000 points/sec. Data from O1–O3 were more accurate estimator of maximum gape analyzed using a Labview™ II virtual in- than minimum gape. Transverse movements strument (written by K. Johnson, Duke Uni- of the mandible in O2 were calculated by plot- versity); data from experiments G1–G2 ting the transverse movement of a lower ca- were analyzed using a Superscope™ II vir- nine marker relative to the mid-sagittal tual instrument (written by D. Lieberman plane. Transverse movements of the mandi- and D. Sadowsky, Rutgers University). Fol- ble in the goat (G2) were calculated by plot- lowing Hylander and Johnson (1993), EMG ting the transverse movement of the left and data were integrated over a 1-msec interval right fourth mandibular incisors relative to with a window of 20 msec, filtered using a the mid-sagittal plane. root-mean-squares (RMS) function, and Rotation of the mandible can be observed then normalized so that the peak values in dorso-ventral projection, but it is difficult during each chewing sequence were 1.0 for to quantify the degree of rotation about the each muscle across one or more documented mandibular axis (symphysis to condyle). In side-shifts. Normalizing the RMS waveform the opossum (O2), rotation was measured across documented side-shifts allows quan- by plotting the medio-lateral distance be- titative comparison between the activity of a 526 D.E. LIEBERMAN AND A.W. CROMPTON single muscle when it is on the balancing vs. TABLE 1. Occlusal wear facet orientations relative to working side (Gorniak and Gans, 1980). Fi- the transverse plane nal analysis of all data was done on Igor Upper second Lower second Pro™ 2.01 (WaveMetrics, Inc., Lake Os- molar molar wego, OR). Using Igor, onset and offset of Species Mean SD n Mean SD n the power stroke were defined as the points Camelus dromedarius 163.5 4.36 4 158.8 2.87 4 Capra hircus 155.8 3.78 4 149.8 5.25 4 at which the wave began to rise or fall Didelphis virginiana 118.5 8.70 4 106.3 6.95 4 steeply from adjacent regions of inactivity. Equus caballus 157.3 4.50 4 158.3 4.27 4 For each power stroke, the area under the Gazella gazella 153.8 6.13 4 142.8 6.75 4 Lama huanachus 153.0 2.45 4 161.3 8.02 4 normalized RMS curve was collected for Lemur fulvus 121.8 1.71 4 117.5 9.04 4 each muscle (calculated as the average am- Macaca fascicularis 154.3 4.65 4 156.3 5.68 4 plitude of the wave times the number of Odocoileus virginiana 153.8 3.95 4 151.0 4.90 4 Procavia capensis 130.5 5.26 4 131.5 4.44 4 points). Rhinceros unicornis 155.3 2.52 3 144.3 12.90 3 As noted above, determination of balanc- Sus scrofa 172.0 3.46 4 173.5 3.70 4 Mean fused 155.11 12.74 27 155.2 13.84 27 ing side and working side (hence side-shifts) Mean unfused 140.7 17.94 20 133.5 19.60 20 was made in three ways. In sequences with cine data (O1, O2, O3, G1, G2), identifica- tion of balancing and working side was made by visual examination of the mastica- tory cycle. For O1 and O3, synchronized an- terior and lateral views of jaw movement were available. For O2, G1, and G2, side- shifts were clearly visible in dorso-ventral cineradiographic films. In O3, determina- tion of side was also confirmed using single- element strain gauges (see Crompton, 1995 for details) bonded to the lateral surface of Figure 1. Box-and-whisker plot (showing mean, standard error, and standard deviation) comparing the the mandible near the ventral margin just 2 orientation of occlusal wear facets of M2 and M relative posterior to the symphysis (i.e., anterior to to the transverse plane of occlusion for five species of the bite point). Gauges in this location reg- mammals with unfused symphyses and eight species ister tensile strain on the working side and with fused symphyses. See text for details of measure- ments and species included. Although there is more compressive strain on the balancing side variation in occlusal angles among mammals with fused (Crompton, 1995). Determination of balanc- symphyses, a Mann-Whitney U-test indicates that the wear facets are significantly (P Ͻ 0.01) more trans- ing and working sides was also confirmed in versely oriented in both the upper and lower molars in the goats, using the differential timing of species with fused than unfused symphyses. the deep and superficial masseters (see Re- sults). During the power stroke in goats as in many other mammals (see Hylander et low-cusped teeth in which grinding occurs al., 1987), the working-side deep masseter with the lower jaw moving primarily medio- and the balancing-side superficial masseter laterally in the transverse (horizontal) consistently fire prior to the balancing-side plane against the upper teeth. An analysis deep masseter and the working-side super- of variation in the occlusal angles in herbi- ficial masseter. This pattern was consis- vores provides general support for this hy- tently observed in the goats, using se- pothesis. Table 1 and Figure 1 provide sum- quences with dorso-ventral cineradiographic mary data on the mean orientations of the data (see Fig. 4). occlusal wear facets of the upper and lower second molars relative to the transverse RESULTS axis of the tooth row for the comparative sample of adult herbivores with fused and Occlusal angle and symphyseal unfused symphyses. A Mann-Whitney morphology U-test indicates that the orientation of oc- Hypothesis 1 predicts that fused symphy- clusal wear facets on the lower molars is on ses evolved convergently in mammals with average 20.3° (P Ͻ 0.005) more transversely WHY FUSE THE MANDIBULAR SYMPHYSIS? 527

TABLE 2. Estimated W/B ratios in Didelphis during mastication of hard foods, with standard deviations in parentheses1 Posterior Middle Anterior Combined Deep Superficial Combined Medial Subject Food Cycles temporalis temporalis temporalis temporalis masseter masseter masseter pterygoid All O1 Beef 9 3.56 (2.06) 1.36 (0.32) 1.97 (1.03) 2.74 0.94 (0.09) 1.34 1.19 1.41 (1.79) (0.32) (0.32) (0.35) O2 Bone 10 1.40 (0.28) 1.32 (0.38) 1.60 (0.60) 1.39 (0.19) 1.69 1.27 (0.19) 1.42 1.37 (0.49) (0.20) (0.13) O3 Bone 10 1.14 1.14 (0.16) 1.14 1.03 1.08 (0.26) (0.20) (0.27) (0.20) O3 Apple 13 1.29 1.44 (1.00) 1.34 0.90 1.07 (0.63) (0.77) (0.23) (0.25) Grand mean 2.48 1.32 1.48 1.68 1.72 1.20 1.31 1.04 1.23 1 W, working-side; B, Balancing-side.

oriented in mammals with fused than un- right-side chews; O3apple comprises 3 side fused symphyses; similarly, the orientation shifts with 6 left-side chews and 7 right-side of upper occlusal wear facets is on average chews. The number of cycles analyzed in 12.6° (P Ͻ 0.0001) more transversely ori- each sequence is limited because the analy- ented in mammals with fused than unfused sis is restricted to chewing cycles in which symphyses. However, it is important to note we were able to verify accurately with cin- from Table 1 that while all species with eradiography and strain gauges the side on unfused symphyses have fairly steep occlu- which the animal was chewing. Figures 2 sal angles, there is more variation among and 3 and Table 2 show that the combined the species with fused symphyses. W/B ratios in the opossum are close to equal, ranging from 1.07–1.41, and averag- W/B EMG adductor ratios ing 1.23. There is, however, some variation Hypothesis 2 predicts that the results of in the W/B ratios among the different ad- Hylander (1979a), in which strain data were ductor muscles and between subjects that is used to infer that primates with an unfused probably related to differences in food hard- symphysis such as the galago recruit pro- ness and bolus position in the oral cavity. In portionately less balancing-side than work- O1beef, for example, the posterior temporalis ing-side adductor muscle force than ma- has the highest average W/B ratio (3.56), caques, are not expected to characterize considerably higher than in O2bone (1.40), most nonprimate mammals with unfused but in some of the individual cycles the ra- symphyses during mastication of hard food. tios are close to 1:1. In addition, W/B ratios This hypothesis is tested with EMG data on are slightly higher in the deep masseter goats and opossums, and compared with than the superficial masseter in all experi- previously published data on macaques ments, with the exception of O3apple. Medial from Hylander et al. (1992). pterygoid activity during the power stroke is the least differential in all experiments, Opossums. Table 2 summarizes descrip- averaging 1.04. The combined W/B ratios of tive statistics for W/B ratios of the summed the deep and superficial masseters are very areas under the normalized EMG waves for similar to the overall W/B ratios for all sub- each muscle and for all working-side and jects. balancing-side muscles from four separate sequences of chews with side shifts from Goats. Table 3 summarizes descriptive O1—O3 (see above). In addition, Figures 2 statistics for the summed areas under the and 3 present side-shift sequences with normalized EMG waves for each muscle and EMG and gape profiles from O1 and O3. for summed values of all working-side and

O1beef comprises 2 side shifts with 4 left-side balancing-side muscles from two separate chews and 5 right-side chews; O2bone com- sequences of chews with side-shifts from prises 2 side shifts with 7 left-side chews each goat. The first G1 sequence includes and 3 right-side chews; O3bone comprises 2 one side shift in which the animal first side shifts with 4 left-side chews and 6 chewed on the right side for 12 cycles and 528 D.E. LIEBERMAN AND A.W. CROMPTON

Figure 2. Jaw movements and muscle activity dur- the normalized root-mean squared EMG values for the ing a sequence of side-shifts from opossum 1 (O1) while temporalis (anterior and posterior compartments), mas- chewing beef chunks. Side-shifts and gape determined seter (deep and superficial compartments), and medial by film (see Materials and Methods). Left- and right- pterygoid. Note that differential working- vs. balancing- side chews denoted as L and R, respectively, at top; side muscle activity occurs mostly in the deep masseter vertical lines denote side-shifts. Plotted are gape and and posterior temporalis. then switched to the left side for 12 cycles. ilar, averaging 1.32, with the deep masseter The second G1 sequence, however, is a syn- showing slightly higher W/B ratios than the thesized side-shift in which the goat first superficial masseter. As in the opossum, the chewed on the left side for 13 cycles, was fed temporalis appears to have the highest W/B more hay, and then chewed on the right side ratios (2.22 and 1.42), but these data come for 16 cycles. The first sequence for G2, il- from only G1, and need to be verified with lustrated in Figure 4, comprises two side- additional studies. shifts with 13 left-side chews and 8 right- side chews; the second G2 sequence Comparison with macaques. Figure 5 comprises one side-shift with 9 left-side plots the W/B ratios for just the combined chews and 8 right-side chews. In both goats, superficial and deep masseters in the goats total W/B ratios for the adductor muscles and opossums with the same type of data sampled range between 1.10–1.37, with a reported by Hylander et al. (1992) for ma- grand mean of 1.23. Combined superficial caques. Because W/B masseter ratios in the and deep masseter W/B ratios are quite sim- macaque are proportional to food hardness, WHY FUSE THE MANDIBULAR SYMPHYSIS? 529

Figure 3. Jaw movements and muscle activity dur- the normalized root-mean squared EMG values for the ing a sequence of side-shifts from opossum 3 (O3) while masseter (posterior deep, anterior deep, and superficial chewing chicken bone. Side-shifts and gape determined compartments) and the medial pterygoid; EMG data by film (see Materials and Methods). Left- and right- were also collected for the digastric and are included side chews denoted as L and R, respectively, at top; here to illustrate abductor muscle activity during the vertical lines denote side-shifts. Plotted are gape and opening stroke.

TABLE 3. Estimated W/B ratios in Capra during mastication of hard foods, with standard deviations in parentheses1 Anterior Deep Superficial Combined Medial Subject Food Cycles temporalis masseter masseter masseter pterygoid All G1 Hay 20 2.22 (2.65) 1.70 1.22 (0.45) 1.34 1.17 1.10 (0.62) (0.35) (1.08) (0.32) G1 Hay 29 1.42 (0.54) 1.17 1.39 (0.42) 1.24 1.19 1.22 (0.25) (0.20) (0.47) (0.20) G2 Hay 21 1.23 1.26 (0.18) 1.24 1.33 1.24 (0.13) (0.10) (0.49) (0.13) G2 Hay 17 1.67 1.20 (0.21) 1.45 1.35 1.37 (0.31) (0.27) (0.38) (0.21) Grand mean 1.82 1.44 1.27 1.32 1.26 1.23 1 W, working-side; B, balancing-side. we plot only the mean W/B ratios for the the data comparable with the goat and opos- higher force levels (4–6) reported by Hy- sum W/B ratios reported here, which come lander et al. (1992; their Table 3) to make from sequences in which hard food was 530 D.E. LIEBERMAN AND A.W. CROMPTON

Figure 4. Jaw movements and muscle activity dur- and eversion are estimated from differential transverse ing a sequence of right-side chews from goat 2 (G2) movement of the medial (solid lines) and lateral (dashed while chewing dry hay. Side-shifts and gape determined line) incisors, as explained in Materials and Methods. by film (see Materials and Methods). Plotted are pre- Four points during the chewing cycle are highlighted: sumptive gape, transverse movement, and inversion MAX, maximum gape; FC/SC, the transition between and eversion of the symphysis, and normalized root- fast and slow close; OC, the temporal midpoint of the mean squared EMG values for the masseter (deep and slow close phase; and MIN, minimum gape. superficial) and medial pterygoid muscles. Inversion

chewed. As Figure 5 shows, the W/B ratios poralis muscles to evert the mandible for the goat and the opossum fall within the during the power stroke. range of the W/B ratios reported for the macaque, with no statistically significant Opossum. Figure 6 plots gape and rota- differences between any of the species. tion of the left and right mandibles around their longitudinal axes in O2 during a side- Mandibular rotation shift while chewing on a chicken bone. Fig- Hypothesis 3 predicts that mammals with ure 6B exaggerates the changing orienta- unfused symphyses tend to rotate their tion of the vertical axis of the mandible mandibles independently during occlusion, (from the mandibular condyle to the ventral unlike mammals with fused symphyses. In margin of the ascending ramus). Note that addition, the medial pterygoid is predicted the ventral margin of the working-side man- to contract biphasically in the goat and the dible tends to evert during the fast close opossum, presumably to invert the mandi- phase prior to the power stroke and then ble prior to occlusion, and then to help con- invert slightly during the power stroke. In trol the tendency of the masseter and tem- contrast, the ventral margin of the balanc- WHY FUSE THE MANDIBULAR SYMPHYSIS? 531 sides during a sequence of right-side chews (immediately followed by a side-shift) (see methods for details). Figure 7 is a schematic of the movements of the symphysis in fron- tal view based on the chewing sequence il- lustrated in Figure 4. In this sequence (not shown in full), the projected transverse dis-

tance between the left I1 and I4 relative to the distance between these teeth during the end of the opening stroke decreased by 0.15 ϭ mm (SD 0.06 mm, n 8), with I4 moving less laterally than I1, which is consistent with inversion of the ventral margin of the mandible. In addition, during the end of the power stroke, between the point of maxi- Figure 5. Comparison of W/B masseter (combined deep and superficial) ratios from O1–O3 and G1–G2 mum intercuspation (OC) and minimum with published hard food (levels 4–6) W/B masseter gape (MIN), the projected distance between ratios from Hylander et al. (1992). An ANOVA finds no the left I1 and I4 decreased by 0.37 mm (SD significant differences between the fused and unfused ϭ species. 0.12 mm, n 8) , with I4 moving less medi- ally than I1, which is consistent with ever- sion of the ventral margin of the mandible. ing-side mandible inverts during fast close Although these data derive from a single and everts considerably during the power experiment, and thus need to be tested us- stroke, presumably because the teeth do not ing additional subjects, they correlate well restrict this rotation. Unfortunately, it is with the differential activity of the medial not possible to calculate absolute degrees of pterygoid and masseter muscles also shown rotation from the film. These data derive in Figure 4 and documented in the other from a single experiment, and thus need to experimental subjects. As in the opossum, be tested using additional subjects, but they the combined activity of the temporalis and correspond to the predicted biphasic activity masseter muscles during the power stroke of the medial pterygoid activity that is doc- not only adducts and shifts the mandibles transversely but, because of their insertion umented in Figure 2 (O1beef), Figure 3 sites laterad to each mandible, also rotates (O3bone), and numerous other sequences (not shown here) in which the medial ptery- them around their longitudinal axes. This goid fires during both the opening and clos- rotation everts the ventral margin of each ing strokes. Similar biphasic medial ptery- mandible. Activity in the medial pterygoids goid activity was previously documented in would tend to counteract this rotation, but O2 by Hylander and Crompton (1986, their medial pterygoid levels are relatively low Fig. 4). during slow close (Fig. 4), with the possible exception of the working-side posterior me- Goat. As noted above, it is more difficult dial pterygoid. to measure mandibular rotation in vivo in Note from the sequence of chews illus- the goat because it is not possible to see the trated in Figure 4 that activity in the bal- lateral border of the mandible in dorso-ven- ancing-side superficial masseter consis- tral view. Nevertheless, preliminary evi- tently precedes that on the working side. dence for independent rotation of the man- This activity tends to move the mandible dibles in G2 is provided by Figure 4, which laterally during fast close, to bring the lower plots the transverse movement of the inner molars into the correct position to engage and outer incisors along with gape, and the upper molars. Moreover, activity in the EMGs from the left and right side deep and working-side superficial masseter consis- superficial compartments of the masseter, tently continues beyond that of the balanc- and from the anterior and posterior com- ing-side masseter, helping to move the man- partments of the medial pterygoids on both dible medially during the power stroke. 532 D.E. LIEBERMAN AND A.W. CROMPTON

Figure 6. Mandibular rotation in the opossum 2 stroke (slow close); FO, fast open; SO, slow open. B: (O2) while chewing chicken bone. A: Gape and rotation Summary schematic of orientations of left and right (inversion vs. eversion) of the ventral margin of the mandibles during a left-side chew, with phases of the mandible during a side-shift. Four phases of the chew- chewing cycle as noted above. Note how working- and ing cycle are highlighted: FC, fast close; PS, power balancing-side mandibles rotate independently.

Figure 4 also shows that there is no signif- Comparative symphyseal morphology icant differential timing in the goat between Hypothesis 4 predicts that the cross-sec- the working- and balancing-side deep mas- tional morphology of the unfused symphysis seters. Apparently, the working-side super- ficial masseter pulls the working-side man- restricts movement in the sagittal plane, to dible medially, whereas the balancing-side allow rapid and complete transfer of dor- deep masseter does little to pull the balanc- sally oriented forces, but should allow some ing-side mandible laterally and help in the degree of independent movement in other side-shift. This pattern differs significantly planes to accommodate the tendency of the from that of the macaque, in which the bal- mandibles to wishbone and rotate around ancing-side deep masseter continues to con- their longitudinal axes as documented tract for at least 26 msec after the working- above. Figure 8 illustrates representative side deep masseter, contributing to transverse sections through an anterior and wishboning (Hylander and Johnson, 1994). posterior region of the mandible of an adult WHY FUSE THE MANDIBULAR SYMPHYSIS? 533 ciently from one mandible to the other, but allowing rotation of each mandible around its longitudinal axis.

Goat. The goat has a typical class III sym- physis (as defined by Scapino, 1981) in which the symphyseal plates are character- ized by interdigitating rugosities. As Figure 8c,d shows, there are significant differences in structure between the anterior, posterior, dorsal, and ventral regions of the symphysis in the goat. A small fibrocartilagenous pad between the two mandibles is present dor- sally at the anterior end of the symphysis (Fig. 8c). This pad acts as the center or rotation for both the twisting of the mandi- bles around their longitudinal axis (condyle to cartilage pad) and independent medio- Figure 7. Schematic anterior view of mandibular lateral transverse movements of the mandi- and symphyseal movement in a goat during one chew- bles. At the anterior end of the symphysis, ing cycle (noted in Fig. 4). Small black dots are ra- diopaque fillings placed in the first and fourth incisors; the medial surfaces of the mandible are large black dot represents the dorsal margin of the roughly parallel to each other and are firmly fibrocartilagenous pad, which acts as a center of rota- connected by the fibrocartilagenous pad and tion. The dashed line is the mid-sagittal plane. MIN, minimum gape; MAX, maximum gape; FC/SC, transi- by numerous densely interlaced cruciate lig- tion between fast close and slow close, which is the aments below. The posterior region of the onset of the power stroke. Note that at both maximum and minimum gape the twisting of the goat symphysis symphysis (Fig. 8d) is dominated by robust decreases the projected (dotted) horizontal distance be- processes (interdigitating rugosities) ar- tween the inner and outer incisors. See text for further ranged to form horizontal ridges which details. project laterally from each symphyseal plate and which interdigitate with depres- opossum, an adult goat, and a juvenile ma- sions in the opposite side. These ridges con- caque. Within each species, little variation sist of heavily vascularized, remodeled was observed between transverse sections bone. The space in between the two symph- from the same region of the mandible and yseal margins, therefore, forms a sigmoid- symphysis. shaped interface in transverse section. The opposing symphyseal plates and their pro- Opossum. As Figure 8a shows, the opos- cesses are bound together by ligaments that sum has a typical class I symphysis (as de- are oriented in a variety of directions, often fined by Scapino, 1981). A fibrocartilag- at right angles to one another (see below). enous pad lies in the antero-dorsal region of As one proceeds posteriorly and ventrally the symphysis, widely separating the two in the goat symphysis, the distance between mandibles and acting as a center of rotation. the mandibles widens and the processes of Ventral to this pad, the two symphyseal the symphyseal plates become increasingly plates are joined by cruciate ligaments, the thicker and more projecting. The orienta- majority of which are dorso-ventrally ori- tion of the ligamentous fibers in between the ented. Posterior to the pad (Fig. 8b), the rugosities is mostly dorso-ventral; towards symphyseal plates in the opossum are also the ventral margin, however, they tend to linked almost entirely by dorso-ventrally run antero-posteriorly through the symphy- oriented cruciate ligaments. Because liga- sis, oriented approximately 45° to either ments are stiff and strong only in their long side of the sagittal plane. At the postero- axis, this orientation ensures stiffness in ventral margin of the symphysis, the two the sagittal plane, thereby ensuring that plates are separated by mostly vascular tis- dorsally oriented forces will transfer effi- sue with a much lower density of randomly Fig. 8. WHY FUSE THE MANDIBULAR SYMPHYSIS? 535 oriented ligaments. The space between the culate species. In the larger herbivorous symphyseal plates, in other words, becomes forms that were present in the early Ter- wider and less fixed along an axis from the tiary and underwent a subsequent adaptive antero-dorsal to postero-ventral ends. At radiation, there is a tendency to either com- the ventral and dorsal margins of the ante- pletely fuse the symphysis or increase the rior end of the symphysis, the two plates are area of contact (e.g., through interdigitating less than 2 mm apart; the symphyseal space rugosities) between the mandibles at the is increasingly wider postero-ventrally, but symphysis. In most mammals (see below for remains narrow close to the dorsal margin. discussion of anthropoids and hyracoids) The orientation of the ligaments and in- there appears to be a good predictive rela- terdigitating rugosities of the goat symphy- tionship between the presence of mandibu- sis described above limits sagittal-plane lar fusion and the movement of the lower movement between the two mandibles, jaw during occlusion. As shown above, thereby permitting the transfer of dorsally mammals with unfused symphyses tend to oriented forces, but these structures permit have occlusal morphologies with steeply some independent twisting and medio-lat- (dorso-ventrally) oriented shearing facets, eral movements of the mandibles relative to which correspond to the primarily dorsally each other (wishboning). However, if the oriented movement of the jaw and molars vertically and obliquely oriented ligaments during the power stroke. In contrast, most between the interdigitating rugosities be- mammals with fused symphyses have sig- come taut during the power stroke, then it is nificantly more horizontally oriented occlu- likely that they stiffen the symphysis in the sal wear facets, reflecting a greater degree transverse plane, helping to transfer hori- of transverse movement of the jaw and teeth zontally oriented force from balancing-side during the power stroke. to working-side mandibles, dragging the In addition, there is evidence that most working-side mandible medially. mammals with unfused symphyses have mandibles that rotate independently during Macaque. The macaque has a typical mastication, in marked contrast to taxa class IV symphysis (as defined by Scapino, with fused symphyses in which such move- 1981). Although the symphysis illustrated ments cannot occur. Independent rotations in Figure 8e,f is a juvenile, the two symph- of the mandible are documented here for the yseal plates are entirely fused with each goat and the opossum, and have also been other, preventing any independent move- documented in carnivorans (Scapino, 1981), ment of the hemimandibles in any plane. insectivorans (Kallen and Gans, 1974; Oron Note that in the posterior end of the sym- and Crompton, 1985), and galagos (Beecher, physis (Fig. 8f), the two mandibles are fused 1977b). These data therefore support the solely by an inferior transverse torus, which hypothesis that, in many mammals, the un- Hylander (1988) has shown to be a likely fused symphysis is primarily an adaptation adaptation to resist wishboning and twist- (or retention) to allow independent move- ing strains. ments of the mandibles during mastication. DISCUSSION As discussed above, mandibular rotation helps to align the cusps of the lower teeth An unfused symphysis is primitive for relative to the upper teeth as they move into Mammalia and is present in all Mesozoic and out of occlusion. In mammals such as mammals. These are predominately insec- the opossum with tribosphenic molars tivorous or small herbivorous, multituber- which have embrasure shearing, the move- ment of the lower molars relative to the upper molars during occlusion is deter- Figure 8. Comparison of coronal sections through re- mined by the angles of the shearing facets, spective anterior and posterior regions of opossum (a, which define the orientation of the embra- b), goat (b, c), and macaque (d, e). FP, fibrocartilag- sures into which the molars fit. The ability enous pad; CL, cruciate ligaments; IR, interdigitating rugosity; TT, transverse torus. See text for detailed to control mandibular rotation may there- descriptions and discussion. fore be necessary to ensure correct orienta- 536 D.E. LIEBERMAN AND A.W. CROMPTON tion of the lower molars relative to the up- the upper molars and vice versa. The angle per molars in order to move into the of occlusion in the goat is between 45–50° embrasures. The slightest misalignment relative to the transverse plane, as the might result in damage to the molar crowns. lower molars move dorso-medially relative In the goat, controlled inversion of the man- to the upper molars (de Vree and Gans, dibles around their longitudinal axes prior 1976). to the power stroke is probably a mecha- Occlusion in taxa with fused symphyses nism for orienting the occlusal plane of the (including anthropoid primates) differs from lower molars parallel with that of the upper occlusion in taxa with unfused symphyses molars. in a number of important respects. First, Independent rotations of the mandibles in taxa with fused symphyses cannot rotate mammals with unfused symphyses are their mandibles independently, even though partly controlled by the activity of the me- the tendency of the adductors to rotate dial pterygoid. The data presented above for (twist) the mandibular corpora around their goats and opossums suggest that the medial long axes generates high symphyseal pterygoid (perhaps only certain compart- strains (Hylander and Johnson, 1994). In ments) tends to fire biphasically in mam- addition, as shown above, most taxa with mals with unfused symphyses, in contrast fused symphyses tend to have relatively to its more typical adductor-like pattern in horizontally oriented wear facets, which re- mammals with fused symphyses. Future re- flect a more horizontally oriented power search, however, is necessary to determine stroke. Medial movement of the jaw on the exactly how much mandibular rotation oc- working side during occlusion in primates curs in goats and opossums, and how these and hyracoids is closer to the horizontal rotations are controlled by the medial ptery- plane than in the goat or other herbivores goid and other muscles such as the lateral that have an unfused symphysis (Janis, pterygoid, the masseter, and the temporalis. 1979a,b; Lucas, 1982). In horses, for exam- The proposed relationship between sym- ple, occlusion takes place through shearing physeal morphology and tooth movements in a single, medially oriented chewing during the power stroke is supported by de- stroke (Lieberman and Crompton, unpub- tailed kinematic work on occlusion in a va- lished data). riety of mammal taxa, including the taxa Viewed in this light, the independent evo- studied here. The opossum, for example, has lution of the fused symphysis in those mam- typical tribosphenic molars in which shear- mal taxa with primarily transversely ori- ing occurs as the trigonid fits tightly into a ented power strokes appears to relate to the V-shaped embrasure between two upper combined function of providing stiffness in molars, with only a small crushing area be- order to transfer force from the balancing- tween the protocone and talonid. Therefore, to working-side mandibles as well as provid- the lower molars move into and out of occlu- ing strength to resist the strains that such sion at a very steep angle (about 80° relative forces generate. As shown in Figure 8 and to the transverse plane) and there is no as noted by previous researchers (Beecher, evidence of any phase II power stroke 1977a, 1979, 1983; Scapino, 1981; Dessem, (Crompton and Hiiemae, 1970; Crompton 1985; Ravosa and Hylander, 1994), the gen- and Kielan-Jaworowska, 1978). A less steep erally vertical arrangement of the cruciate orientation of occlusion characterizes the ligaments (and, when present, the interdig- goat, in which a double set of antero-poste- itating rugosities) that bind the unfused riorly aligned lophs on the lower molars symphyseal plates, clearly creates stiffness shears past a similar double set on the up- in the sagittal plane by restricting dorso- per molars as the working-side mandible ventral shearing movements, but allows moves medio-dorsally during occlusion some degree of lateral transverse bending (Smith and Savage, 1959). Occlusion occurs and twisting around the long axes of the as the high points of the cusps on the lower mandibles. Fusion is an obvious “solution” molars shear down the transversely ori- to the problem of how to transfer medially ented valleys formed between the cusps of directed forces rapidly and completely WHY FUSE THE MANDIBULAR SYMPHYSIS? 537 across the symphysis. Fusion prevents perficial masseters are not significantly dif- transverse bending and independent rota- ferent from those of the macaque. In the tion of the mandibles, but perhaps gener- goat and the opossum, combined adductor ates higher wishboning and twisting W/B ratios average about 1.2:1; combined stresses. Increased symphyseal mass will W/B ratios for the deep and superficial mas- reduce the strains generated in all planes seters average about 1.3:1. Weijs and Dan- (Ravosa and Hylander, 1994). This principle tuma (1981) found that W/B adductor ratios may explain why, in carnivores, there is a in lagomorphs that have an unfused sym- tendency for larger-bodied species (especial- physis are also close to 1:1. Hylander et al. ly felids and ursids) to have more rigid or (2000), however, showed that W/B ratios in “partially fused” symphyses than smaller- the galago for the combined masseters is bodied species (Scapino, 1981). Ravosa 3.3:1, but almost all of this difference is (1991) documented a similar trend among caused by an extremely high W/B ratio prosimians in which longer-jawed species (4.4:1) for the deep masseter. The EMG data have wider, more rigid symphyses than presented here, therefore, do not support shorter-jawed species. It is important to the hypothesis that, as a rule, mammals note, however, that such size-related trends with unfused symphyses recruit proportion- appear to be lineage-specific. There is no ately less adductor force from balancing- evidence, for example, for any size-related side muscles than mammals with fused effects on symphyseal fusion in bovids, symphyses. The only major difference may probably because of the importance of man- be in those muscles that play a major role in dibular rotation during occlusion (see generating transverse force (see below). above). Based on the experimental data pre- It seems likely that the unfused symphy- sented here, we predict that, as a general sis can be quite stiff in the sagittal plane: in rule, most mammals with fused and un- the goat this stiffness is provided by inter- fused symphyses recruit equal amounts of digitating rugosities; in the opossum this dorsally oriented balancing-side and work- stiffness is mostly a function of the arrange- ing-side adductor force, at least when chew- ment of the cruciate ligaments. Since the ing hard food. However, hypotheses 2–4 are unfused symphysis probably transfers dor- sally oriented force as completely as the tested here with only a small number of fused symphysis (see Dessem, 1985), it fol- taxa. We stress that more experimental lows that mammals with unfused and fused data on mastication are needed for more symphyses are expected to have similar taxa with fused and unfused symphyses. In overall W/B adductor ratios as measured by particular, additional EMG data from pros- EMGs. Gorniak and Gans (1980) showed imians are needed to test more completely that EMG levels normalized across side- the hypothesis that anthropoids recruit shifts are reasonable indicators of the force more balancing-side force during mastica- generated by the adductor muscles. There- tion than prosimians. As noted above, Hy- fore, equal activity in the same muscle when lander et al. (2000) showed that W/B ratios chewing on the balancing and working side in the galago are higher than those reported means they are generating the same con- for other anthropoid primates for the super- tractile force. To date, most of the direct ficial masseter, primarily because of differ- EMG data on W/B adductor force ratios in ential activity in the deep masseter. Given mammals with fused symphyses come from the importance of the deep masseter in pri- macaques and humans, in which masseter mates for generating transverse movement W/B ratios tend to approach 1:1, depending during the power stroke, these data there- on food hardness and bite location (Hy- fore support the hypothesis that symphy- lander et al., 1987; Spencer, 1995, 1998). seal fusion is an adaptation for generating The data presented above from goats and transverse movement in anthropoids (Hy- opossums indicate that, in these species, lander et al., 2000). Along this vein, EMG W/B ratios for the combined adductor mus- data from nonprimates with fused symphy- cles as well as the combined deep and su- ses are necessary to determine if these taxa 538 D.E. LIEBERMAN AND A.W. CROMPTON have higher W/B ratios than goats or opos- not among other taxa in which mandibular sums. rotation is known to occur during the power These interpretations raise some interest- stroke. To test this hypothesis more fully, ing questions regarding the evolution of however, more data are needed on W/B symphyseal fusion in primates and hyraxes, EMG adductor ratios and the extent to and the hypothesis that symphyseal fusion which the mandibles rotate independently in anthropoids is an adaptation to during the power stroke in prosimians. strengthen as well as stiffen the symphysis CONCLUSIONS (see Ravosa and Hylander, 1994). As noted above, W/B strain ratios in the galago aver- Fusion of the mandibular symphysis ap- age 3.5:1 in the mandibular corpus, whereas pears to be a function primarily of the move- W/B strain ratios are roughly 1.5:1 in the ments of the teeth during occlusion. Mam- macaque, suggesting that galagos recruit mals with predominantly vertically oriented less balancing-side adductor force than ma- occlusal wear facets on their teeth tend to caques (Hylander 1979a,b; Ravosa and Hy- have unfused mandibular symphyses, in lander, 1994). If strain ratios are represen- which the two mandibles rotate indepen- tative of muscle force ratios, then one would dently of one another during the power expect the pattern of muscle recruitment stroke. Since an unfused symphysis proba- and/or force transfer across the symphysis bly transfers dorsally directed force as well to be different in prosimians than in the as a fused symphysis, most mammals with other mammals with unfused symphyses. unfused symphyses appear to have similar The EMG data reported above for galagos levels of adductor activity on their working- (Hylander et al., 2000), in which galagos and balancing-side muscles, as documented have a significantly higher W/B ratio for the here for the goat and the opossum. In this deep masseter compared not only with an- respect, there appears to be no difference in thropoids but also with the goat and the balancing-side to working-side adductor opossum, suggest this to be the case. It is muscle ratios between nonprimates with therefore possible that the pattern of bal- unfused symphyses and the macaque, ancing-side adductor muscle recruitment which has a fused symphysis. and force transfer across the symphysis is Mammals such as anthropoids with different in primates, especially prosimians, transversely oriented occlusal wear facets than in many mammalian taxa. As sug- on their teeth tend to have fused mandibu- gested by Hylander (1979a) and Ravosa and lar symphyses, which restrict transverse Hylander (1994), prosimians such as the ga- bending. These mammals also tend to have lago may not recruit as much balancing-side power strokes in which there is little inde- adductor force as higher primates or other pendent movement (especially rotation) al- mammals with unfused symphyses for rea- lowed between the working- and balancing- sons that relate to differences in diet. In side mandibles, in spite of the tendency of addition, if prosimians, like some car- many of the adductor muscles to evert the nivorans, have little mandibular rotation ventral margin of the mandible during the and thus have no need to maintain an un- power stroke. Mandibular fusion in these fused symphysis, then a fused symphysis in taxa is probably an adaptation primarily to primates may have evolved as an adapta- increase the speed and completeness with tion “to resist structural failure from the which transverse force transfers across the increased symphyseal stress resulting from symphysis. Mandibular fusion also helps to increased recruitment of balancing-side strengthen the mandibular symphysis, per- jaw-muscle force during mastication” (Ra- haps because higher wishboning and twist- vosa and Hylander, 1994, p. 451). 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