Taylor AB, Vinyard CJ, 2013. The relationships among jaw-muscle fiber architecture, jaw morphology,...

The Relationships Among Jaw-Muscle FiberArchitecture, Jaw Morphology, and Feeding Behavior inExtant Apes and Modern Humans

Andrea B. Taylor1,2* and Christopher J. Vinyard3

1Department of Community and Family Medicine, Doctor of Physical Therapy Program, Duke University School ofMedicine, Durham, NC 277082Department of Evolutionary Anthropology, Duke University, Durham, NC 277083Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, OH 44272-0095

KEY WORDS masseter; temporalis; hominoids; diet; evolution

ABSTRACT The jaw-closing muscles are responsiblefor generating many of the forces and movements associ-ated with feeding. Muscle physiologic cross-sectional area(PCSA) and fiber length are two architectural parametersthat heavily influence muscle function. While there havebeen numerous comparative studies of hominoid andhominin craniodental and mandibular morphology, littleis known about hominoid jaw-muscle fiber architecture.We present novel data on masseter and temporalis inter-nal muscle architecture for small- and large-bodied homi-noids. Hominoid scaling patterns are evaluated andcompared with representative New- (Cebus) and Old-World (Macaca) monkeys. Variation in hominoid jaw-mus-cle fiber architecture is related to both absolute size andallometry. PCSAs scale close to isometry relative to jawlength in anthropoids, but likely with positive allometryin hominoids. Thus, large-bodied apes may be capable of

generating both absolutely and relatively greater muscleforces compared with smaller-bodied apes and monkeys.Compared with extant apes, modern humans exhibit areduction in masseter PCSA relative to condyle-M1 lengthbut retain relatively long fibers, suggesting humans mayhave sacrificed relative masseter muscle force duringchewing without appreciably altering muscle excursion/contraction velocity. Lastly, craniometric estimates ofPCSAs underestimate hominoid masseter and temporalisPCSAs by more than 50% in gorillas, and overestimatemasseter PCSA by as much as 30% in humans. Thesefindings underscore the difficulty of accurately estimatingjaw-muscle fiber architecture from craniometric measuresand suggest models of fossil hominin and hominoid biteforces will be improved by incorporating architecturaldata in estimating jaw-muscle forces. Am J Phys Anthro-pol 151:120–134, 2013. VC 2013 Wiley Periodicals, Inc.

Jaw muscles are functionally important for generatingthe masticatory movements and occlusal forces associ-ated with ingestion, biting and chewing. Despite theirfunctional significance, we know relatively little aboutthe functional anatomy of the jaw muscles in hominoids(Gregory, 1950; G€ollner, 1982; Wall et al., 1994). Amongthe structural characteristics of muscle, fiber architec-ture is an important determinant of muscle function.Fiber architecture refers to the arrangement of musclefibers relative to the force-generating axis of the muscle(Gans and Bock, 1965). Given two muscles of comparablevolume (and holding other non-architectural factors con-stant), a parallel-fibered muscle will comprise long fibersthat are oriented parallel to the axis of force generation.Because the total distance a fiber can shorten equals thesummed shortening distances of the sarcomeres in series(i.e., overlapping actin and myosin filaments) (Lieber,2010), parallel-fibered muscles are well suited to maxi-mizing excursion and contraction velocity (Bodine et al.,1982). Alternatively, muscles with pinnate fibers thatare oriented at an angle relative to the force-generatingaxis can pack more, albeit shorter, fibers in a givenspace. Because a muscle’s physiologic cross-sectionalarea (PCSA) is proportional to its maximum force-gener-ating capacity (Powell et al., 1984), pinnate-fiberedmuscles are well suited to generating force. Other fac-tors being equal, there is a theoretical architecturaltrade-off between PCSA and fiber length, such that amuscle cannot be efficiently optimized for both force pro-duction and excursion/contraction velocity (Gans and

Bock, 1965; Taylor and Vinyard, 2004; Taylor et al.,2009).

We compare masseter and temporalis muscle fiberarchitecture in a sample of small- and large-bodied hom-inoids. Specifically, we evaluate absolute and relativevariation as well as scaling patterns in hominoidjaw-muscle architecture and compare hominoids withrepresentative New- (e.g., Cebus) and Old-World(e.g., Macaca) monkeys. In addition to furthering ourunderstanding of how jaw-muscle architecture is

Additional Supporting Information may be found in the onlineversion of this article.

Grant sponsor: National Science Foundation; Grant numbers:BCS 0452160, BCS 0635649, BCS 0833394, BCS 0552285, BCS0962677, Grant sponsor: National Institutes of Health; Grant num-ber: NSMRC R24 HD050837-01; Grant sponsor: Duke Undergradu-ate Research Support Office.

*Correspondence to: Andrea B. Taylor, Department of Communityand Family Medicine, Doctor of Physical Therapy Program, DukeUniversity School of Medicine Box 104002, Durham, NC 27708,USA. E-mail: [email protected]

Received 19 June 2012; accepted 11 February 2013

DOI: 10.1002/ajpa.22260Published online 3 April 2013 in Wiley Online Library

(wileyonlinelibrary.com).

� 2013 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 151:120–134 (2013)

functionally and evolutionarily adapted to feedingbehaviors across primates, we also can begin to addressspecific questions related to hominoid feeding behaviorand evolution.

Our sample sizes are small, particularly for the large-bodied hominoids. Moreover, there are scant data onhominoid ingestive and masticatory behaviors as well asthe structural and material properties of the foods theyprocess (e.g., Elgart-Berry, 2004; Taylor et al., 2008;Vogel et al., 2008). Nonetheless, we draw on the avail-able data to develop functional questions and testhypotheses. Interpretations and conclusions based onthese results should be validated by additional studiesincorporating larger samples and improved data on feed-ing behaviors.

Question 1: Do the force-generating capacities of themasseter and temporalis muscles correspond with man-dibular load-resistance abilities across hominoids?Although the functional correlates of hominoid jaw formand feeding behavior have been well studied (Groves,1970; Daegling, 1989, 2001, 2007; Daegling and Grine,1991; Uchida, 1996; Brown, 1997; Taylor, 2002, 2005,2006a,b; Taylor et al., 2008), we do not know how closelythe force-generating capabilities of the jaw-closingmuscles correspond to mandibular load-resistance abil-ities. While we lack comprehensive data on the mechani-cal properties of the foods ingested and masticated byhominoids, the limited dietary data available suggestthat orangutans and gorillas process mechanically morechallenging foods than chimpanzees, hylobatids, andhumans. Based on these potential differences in foodproperties, we hypothesize that relatively larger musclePCSAs (after accounting for load-arm lengths) shouldgenerate relatively larger external forces and internalloads in the mandible. These elevated internal loadsshould be associated with improved load resistance abil-ities through increases in size and/or shape of the man-dibular corpora, symphyses, and/or condyles. Thus, wepredict a correlation between relative PCSA and relativejaw load-resistance ability across hominoids.

Question 2: Do we observe an architectural trade-offbetween the capacities for maximum force-generationand maximum excursion/contraction velocity of themasseter and temporalis? Muscles with larger PCSAstend to comprise shorter, more pinnate fibers as fiberlength is inversely proportional to PCSA. Alternatively,longer-fibered muscles facilitate larger muscle excur-sions and increased contraction velocities. Given an ini-tial prediction that masseter and temporalis fiberarchitecture should be patterned to improve muscle (andbite) forces in hominoid taxa with mechanically chal-lenging diets (e.g., orangutans and gorillas), we askwhether there is an architectural trade-off between max-imizing force (PCSA) versus maximizing excursion/con-traction velocity (Lf). We have no ecological orbehavioral evidence to predict differences in maximumexcursion/contraction velocity among hominoids. There-fore, in taxa with relatively smaller PCSAs, we wouldinitially interpret the presence of relatively longer fibersas an architectural trade-off between maximizing forceversus excursion/contraction velocity.

Question 3: Does the hominoid radiation involve sub-stantial evolutionary changes in jaw-muscle fiber archi-tecture? Hominoids, with some exceptions, retain aprimitive molar morphology compared with cercopithe-coids, but have evolved considerable variation in locomo-tor behavior and postcranial morphology (Andrews,

1985). This mosaic pattern led to suggestions that ifchanges in feeding behavior and diet played a significantrole in the adaptive radiation of hominoids, then theability to adopt new foraging strategies and exploit dif-ferent resources was met primarily via alterations inlocomotor strategies (Ripley, 1979; Temerin and Cant,1983). We compare fiber architecture of the masseterand temporalis muscles in hominoids to representativeMacaca and Cebus species to assess potential evolution-ary changes in the architectural arrangements of thesemuscles. If hominoids systematically differ from thesemonkeys in jaw-muscle fiber architecture, it would pro-vide support for the hypothesis that feeding behaviorand diet factored significantly in the hominoid adaptiveradiation.

Lastly, we provide data on hominoid jaw-muscle fiberarchitecture to support biomechanical models of thehominoid masticatory apparatus. Bite force is an impor-tant criterion of masticatory performance and efficiency(Kurita et al., 2001) but for practical reasons, in vivobite force measurements are difficult to obtain in non-human hominoids. Calculated bite forces based on esti-mates of muscle forces and moment arms can provide areasonable alternative to empirically measured biteforces. To date, bite force estimates for hominoids largelyderive from mechanical models that relied on skeletalcorrelates to estimate muscle force (Demes and Creel,1988; O’Connor et al., 2005) and/or electromyographicdata from anthropoid jaw-muscle recruitment patterns(Strait et al., 2007; Taylor et al., 2008). More recently, ithas become standard to generate three-dimensional bio-mechanical models of the masticatory apparatus usingfinite-element analysis (Strait et al., 2005; Wroe et al.,2010; Cobb and Panagiotopoulou, 2011; Tseng et al.,2011; Cox et al., 2012). Importantly, the accuracy ofthese methods for modeling how a complex structurelike the skull behaves under various loading conditionsdepends on the validity of the input parameters, includ-ing muscle forces (Strait et al., 2005; Tseng et al., 2011).We continue to build on this previous work by providingadditional muscle architectural data for these types ofmodels of hominoid feeding behaviors.

MATERIALS AND METHODS

Samples

We examined the masseter and temporalis muscles inHylobates sp. (H. lar, n 5 1; H. syndactylus, n 5 2), Pongopygmaeus (n 5 2), Gorilla gorilla (n 5 4), Pan troglodytes(n 5 5), and Pan paniscus (n 5 1).1 We also examinedmuscles in representative Old- (Macaca fascicularis,n 5 1 and M. mulatta, n 5 3) and New-World (Cebus albi-frons, n 5 5 and C. capucinus, n 5 3) monkeys (Support-ing Information Table 1). We used previously publisheddata for Cebus (Taylor and Vinyard, 2009a) and humans(van Eijden et al., 1997). All non-human primates werecaptive specimens and dentally adult based on thirdmolar eruption. Tissue was either previously frozen, orfixed and stored in formalin or ethanol. We fixed frozentissue and subsequently stored all harvested muscles in10% buffered formalin.

1Not all specimens had both masseter and temporalis muscles (seeSupporting Information Table 1).

JAW-MUSCLE ARCHITECTURE IN HOMINOIDS 121

American Journal of Physical Anthropology

Data collection

We removed the skin and superficial fascia overlyingthe jaw muscles and measured whole masseter and tem-poralis lengths in situ. These and all other linear dimen-sions of the mandible and jaw musculature weremeasured using digital calipers accurate to the nearest0.01 mm. Muscles were dissected free from their bonyattachments, trimmed of excess tendon and fascia, blot-ted dry, and weighed to the nearest 0.01 g. We weighedthe superficial and deep portions of the masseter sepa-rately; however, only the superficial masseter was usedfor analysis.2 We measured jaw length from the posterioredge of the condyle to infradentale and condyle-M1

length from the posterior edge of the condyle to the ante-rior margin of M1.

Fiber length and pinnation angle were measured forboth muscles following Taylor et al. (2009) and Taylorand Vinyard (2009a). We sectioned the masseter andtemporalis along their lengths (Fig. 1). In sectioning thetemporalis, we produced anterior, middle, and posteriorsegments. Depending on the size of the masseter muscle,we produced a minimum of two and a maximum ofseven segments, each approximately 1.5 cm in thickness.We oriented each segment to view fibers in cross-section,pinned the segment to a Styrofoam block, and visualizedthe proximal and distal attachments of individual fibersto tendon (Fig. 1) using a 5 diopter (2.253) magnifierlight. We selected anterior and posterior sampling sitesalong the length of the masseter (Fig. 1a), and proximaland distal sampling sites for the temporalis (Fig. 1b). Ateach sampling site, we measured five to six fibers. Thus,depending on the species and the number of muscle seg-ments, we measured 10 to 72 fibers per muscle. For eachfiber, we measured fiber length (Lf) between the proxi-mal and distal myotendinous junctions (Fig. 1).

Because specimens were fixed at different gapes, wenormalized measured fiber lengths to a standardizedsarcomere length (Felder et al., 2005). After measuringfiber lengths, muscle segments were chemically digestedin 30% HNO3 and saline solution (Loeb and Gans, 1986)until the surrounding connective tissue could beremoved and fiber bundles easily separated. Fiber bun-dles from each muscle were dissected in 13 PBS undera dissecting microscope (Nikon SMZ1500). Five to 10small fiber bundles were mounted on slides, cover-slipped with mounting medium (Cytoseal) and left to airdry. We measured sarcomere lengths (Ls) from thesefiber bundles using laser diffraction which relies on inci-dent laser light diffracting through the I-band region ofthe sarcomere to estimate sarcomere length (to the near-est 0.01 lm) (Lieber et al., 1984). We normalized in situfiber lengths for the non-human primate sample to aresting fiber length using the following equation:

NLf 5 Lf 2:41 lm=Lsð Þ;

where NLf is normalized fiber length, Lf is measuredfiber length, Ls is measured sarcomere length, and 2.41mm is the empirically determined optimal sarcomerelength for non-human primate lower limb muscle(Walker and Schrodt, 1974).

Using these measurements, we computed the followingvariables for each individual:

1. Mean normalized fiber lengths (NLf) for the superfi-cial masseter and temporalis, estimated as the aver-age of all fibers sampled from a muscle. Meannormalized fiber length for each muscle was used inall subsequent calculations involving fiber length.

2. Pinnation angle (u) computed as the arcsine a/NLf(Anapol and Barry, 1996) (Table 1; Fig. 1). Pinnationangle was computed for each fiber and then averagedacross all fibers for a given muscle per specimen.

3. Physiological cross-sectional area (PCSA), computedas:

PCSA cm 2� �

¼ muscle mass gmð Þ3cos u

NLf cmð Þ 3 1:0564 gm =cm 3ð Þ ;

where 1.0564 gm/cm3 is the estimated specific density ofmuscle (Mendez and Keys, 2011).

Fiber architecture data for modern Homo sapiens aretaken from van Eijden et al. (1997). These authors pro-vide data on fiber bundle length (Lf), in situ measuredsarcomere length (Ls) and pinnation angle (h). However,they did not normalize Lf by Ls and did not incorporatepinnation angle in their estimates of PCSA. Therefore,we used the average in situ sarcomere length measure-ments for the masseter (Ls 5 2.47 mm) and temporalis(Ls 5 2.33 mm) from van Eijden et al. (1997) to normalizetheir Lf estimate as previously described, and recom-puted human PCSAs incorporating NLf and reportedpinnation angle using the above equation.3 We normal-ized the human data by an optimal sarcomere length of2.72 mm (the average of empirically determined optimalsarcomere lengths for human lower limb [2.64 mm;Walker and Schrodt (1974)] and human wrist extensor[2.80 mm; Lieber et al., 1994] muscles).

Data analysis

We used nonparametric Kruskal–Wallis tests to evalu-ate statistical differences among taxa and followed a sig-nificant result with pairwise Mann–Whitney U tests toassess differences between species. We evaluated differ-ences in whole muscle mass, absolute PCSAs, fiberlengths (NLf), and pinnation angles. To examine relativedifferences, we created ratios by dividing NLf and PCSAby jaw length and condyle-M1 length.4 Jaw length wasused as an estimate of the load arm for incision whereascondyle-M1 length was used as an estimate of the loadarm for biting at M1. We further divided PCSA0.5 by jawlength and by condyle-M1 length to create dimensionlessvariables for comparison.

We excluded any group of n< 3 from pairwise statisti-cal analysis among species, thereby eliminating Pongo,P. paniscus, and Homo (where we used a previously pub-lished mean value; n 5 1). We combined our hylobatidsample (H. lar and H. syndactylus) for statistical

2Where possible, we averaged right and left muscle weights andused these averages in all variables involving muscle mass.

3We observed a 27.3% difference for masseter PCSA, and 21.6% dif-ference for temporalis PCSA, between published values by van Eijdenet al. (1997) and our normalized estimates.

4We did not measure condyle-M1 length on each specimen. There-fore, we used measurements from Taylor (2002, 2006b, unpublisheddata), Vinyard (unpublished data), and Terhune (unpublished data) tocompute means for each group.

122 A.B. TAYLOR AND C.J. VINYARD


purposes but treated them separately in scaling analyses(see below). Statistical tests among groups focused onthe masseter. Lastly, as our small sample sizes reducestatistical power, in this initial analysis we highlightfindings that trend toward significance (0.05<P< 1.0)and do not apply a post hoc adjustment for Type I errorprobabilities.

To evaluate the interspecific allometric and evolution-ary changes of fiber architecture, we examined the scal-ing relationships of NLf and PCSA relative to jaw lengthand condyle-M1 length. We initially considered phyloge-netic generalized least squares (PGLS) (Freckletonet al., 2002) using a random sample of 100 dated phylog-enies (Arnold et al., 2010) (10kTrees V. 3; available at:http://10ktrees.fas.harvard.edu). Our estimate of phylo-genetic correlation (k) was not significantly differentfrom 0 (P>0.05), indicating an absence of phylogeneticsignal, and significantly different from 1 (P< 0.05; wherek 5 1 suggests a phylogenetic signal) in six of eight scal-ing analyses. In the remaining two regressions, k 5 0 butwas not significantly different from 0 or 1 (P> 0.05) sug-gesting limited statistical power. Given the absence ofphylogenetic signal in these analyses, we examined scal-ing relationships using natural log-transformed varia-bles and reduced major axis (RMA) regression (Rayner,1985). Importantly, all regressions generated usingPGLS remained significant and the pattern of regression

coefficients was similar using both PGLS and RMAapproaches.

Finally, to evaluate the relationship between relativemaximum muscle force production and relative load re-sistance ability, we compared relative masseter PCSA0.5

to an estimate of mandibular load resistance abilityacross species. To estimate load resistance ability, weaveraged measures from the corpus (M1 corpus depthand width), symphysis (depth and width), and condyle(length and width) for each species.5 Because we lacktemporalis data for some species, we used masseterPCSA0.5 to estimate relative maximum force production.Both muscle force and the average of load resistancemeasures were divided by mandible length and condyle-M1 length, respectively, to generate dimensionless shaperatios. We calculated Pearson’s product moment correla-tions between these variables for raw data as well asphylogenetic independent contrasts (PIC). PIC were esti-mated in the PDAP: PDTree module (Midford et al.,2005) of Mesquite (V. 2.73, Maddison and Maddison,2010) based on a consensus phylogeny (10kTrees V.3).We confirmed that absolute values of standardized PICdata for each variable were not correlated with the

Fig. 1. Muscle cross-sections of a) male chimpanzee left masseter (Specimen# CJV 187) and b) male chimpanzee right tempora-lis (Specimen# Zur 8764). The central schematic of ape skull in lateral view depicts in situ masseter (dotted black arrow) and tem-poralis (solid black arrows) orientation. Muscles were sectioned along their lengths approximately every 1.5 cm, from posterior toanterior for the masseter (dotted black arrow) and from distal to proximal for the temporalis (solid black arrows). For both musclecross-sections, the solid black line represents individual fiber lengths (Lf), running from the central to the distal tendon. The myo-tendinous junction (MTJ) is the region where fibers attach to the central tendon. The black dotted line represents the perpendicu-lar distance (a) from muscle edge to the central tendon. For each muscle cross section, a minimum of five fibers was sampled fromthe anterior masseter and proximal temporalis (white-filled red dot), and from the posterior masseter and distal temporalis (white-filled blue dot). Fiber length (Lf) was normalized for sarcomere length and pinnation angle then was computed as the arcsine of a/NLf.

5Corpus, symphysis, and condylar measurements are from Taylor(2002, 2006b, unpublished data) for Hylobates, Pongo, Pan, and Go-rilla and from Vinyard (unpublished data) for Homo.



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standard deviation of branch lengths (Diaz-Uriarte andGarland, 1998). While we focus on shape ratios based onthe average load resistance ability for each species, weinclude correlations with each mandibular measure inSupporting Information Table 2. Raw statistics and plotswere generated using Systat 11.0VR .

RESULTS

Gross morphology of the masseter andtemporalis muscles

The gross morphology of the masseter and temporalismuscles in hominoids is similar to other primates(Ant�on, 1999; Taylor et al., 2009; Taylor and Vinyard,2009a,b) and non-primate mammals (Turnbull, 1970).The masseter is multipinnate and comprises a large su-perficial portion and a much smaller deep portion. Simi-lar to other anthropoids, the posterior deep masseterfibers approximate a vertical orientation, nearly perpen-dicular to the superficial masseter fibers, and maintain atransverse orientation relative to the jaw. The fan-shaped temporalis is bipinnate, larger than the massetermuscle in all species examined here, and has superficialand deep portions separated by an intramuscular tendon(Table 1). Consistent with our previous studies of pri-mate jaw muscles (Taylor et al., 2009; Taylor and Vin-yard, 2009a), pinnation angles are larger in thehominoid masseter (9.6�–21.5�) compared with tempora-lis (8.8�–16.2�) (Table 1).

Relative masseter PCSA and relative jawrobusticity

Among hominoids, the correlation between load resist-ance ability and masseter PCSA0.5 is not significantwhen considered relative to jaw length (raw r 5 0.55,P 5 0.2; PIC r 5 0.35, P 5 0.44) (Fig 2a). Alternatively,we see evidence for an association between load resist-ance ability and masseter force production when

considered relative to condyle-M1 length (raw r 5 0.76,P 5 0.048; PIC r 5 0.73, P 5 0.06) (Fig. 2b). Thus, ourresults suggest a potential relationship between relativemuscle force and mandibular morphology that may bemore closely related to molar biting and potentially mas-tication compared with behaviors involving anteriortooth use.

Absolute variation in fiber architecture

Muscle weight clearly distinguishes the small-bodiedhominoids and monkeys from the large-bodied hominoids(excluding Homo), with Gorilla at the extreme end ofthe size range (Table 1 and Fig. 3). Gorilla superficialmasseter muscle mass is nearly 50 times that of thesmallest monkey, Cebus, and three times the mass ofPan troglodytes (Table 1 and Fig. 3). In hominoids, mus-cle mass generally tracks absolute PCSA and specieswith the largest masses and PCSAs also tend to havethe absolutely longest fibers. P. troglodytes, however, hasa smaller temporalis PCSA, but longer temporalis fiberscompared with Gorilla (Table 1). Non-parametric com-parisons for the masseter support these significant size-related increases in architectural dimensions amonglarge-bodied hominoids and between hominoids andmonkeys (Table 2). There are no significant differencesin pinnation angle among species for either the masseter(Kruskal–Wallis test: H 5 4.10, df 5 4, P 5 0.39) or tem-poralis (H 5 7.37, df 5 4, P 5 0.12).

Anapol et al. (2008) are the only investigators toreport jaw-muscle fiber architecture for non-human hom-inoids. Using similar methods, their normalized PCSAestimate for Hylobates (1.91 cm2) is comparable to ournormalized PCSA estimate for H. lar (1.75 cm2), whereastheir normalized PCSA estimate for Symphalangus (1.29cm2) is considerably lower than ours (6.02 cm2) (see Sup-porting Information Table 1). In addition to variabilityin sample preservation, individual differences in musclearchitecture affecting sample composition, such as size,

Fig. 2. Bivariate plots of the relationship between relative load resistance ability and relative masseter PCSA0.5 in hominoids.Shape variable comparisons relative to jaw length (A) do not indicate an association. Correlations relative to condyle-M1 length (B)suggest a significant relationship between the force-producing capacity of the masseter and mandibular load resistance abilityamong hominoids. “Raw r” indicates product moment correlation for species data and “PIC r” indicates correlation using phyloge-netic independent contrasts.



age, gender and/or muscle plasticity, likely contribute tothese disparate results. This variation emphasizes theneed for continued evaluation of hominoid, and morebroadly primate, jaw-muscle fiber architecture.

Relative differences in fiber architecture

Relative PCSA. The apes show considerable overlap inrelative masseter and temporalis PCSAs with the excep-tions of the distinctively large temporalis PCSA in Gorillaand relatively small PCSAs in H. lar (Table 1 and Fig. 4a).Orangutans, gorillas and chimpanzees have greater aver-age masseter and temporalis PCSAs relative to jaw length

compared with the smaller-bodied gibbons and humans(Table 1 and Fig. 4a). We observe a similar pattern in com-parisons of masseter PCSA relative to condyle-M1 length(not shown). Given the similarities in pinnation angles,we attribute observed differences in relative PCSAslargely to changes in jaw-muscle mass. A similar patternis seen between untufted and tufted capuchins (Organet al., 2009; Taylor and Vinyard, 2009a).

There are no significant (H 5 2.47, df 5 4, P 5 0.65) dif-ferences in PCSA0.5/jaw length among species as thedegree of interspecific overlap increases considerablyonce the effect of area is removed with these scale-freeratios (Table 2 and Fig. 4b). For example, the 10-fold

Fig. 3. Superficial masseter cross-sections from left to right of adult G. gorilla (Specimen# CMNH 23), P. troglodytes (Speci-men# CJV 187), H. syndactylus (Specimen# Zur 7292), and C. capucinus (Specimen# NMNH 257972). Gorilla superficial massetermuscle mass is nearly 50 times that of the smallest monkey, Cebus, and three times the mass of P. troglodytes (see also Table 1and Supporting Information Table 1).

TABLE 2. Results of nonparametric Mann–Whitney U tests for absolute and relative differences in masseter architecturalvariablesa,b,c

SuperficialMasseter muscle

mass (g)

SuperficialMasseterNLf (mm)

SuperficialMasseter

PCSA (cm2)

SuperficialMasseter

PCSA/Jawlength

SuperficialMasseter

PCSA0.5/Jawlength

SuperficialMasseterNLf/Jawlength

Pan vs. Gorilla 0.0143 (P<G) 0.0275 (P<G) 0.0143 (P<G) 0.0860 (P<G) NS NSPan vs. Hylobates 0.0253 (P>H) 0.0253 (P>H) 0.0526 (P>H) NS NS NSPan vs. Macaca 0.0143 (P>M) 0.0143 (P>M) 0.0143 (P>M) 0.0860 (P>M) NS NSPan vs. Cebus 0.0034 (P>C) 0.0045 (P>C) 0.0045 (P>C) 0.0280 (P>C) NS NSGorilla vs. Hylobates 0.0339 (G>H) 0.0339 (G>H) 0.0339 (G>H) 0.0339 (G>H) NS NSGorilla vs. Macaca 0.0209 (G>M) 0.0209 (G>M) 0.0209 (G>M) 0.0209 (G>M) NS NSGorilla vs. Cebus 0.0066 (G>C) 0.0082 (G>C) 0.0082 (G>C) 0.0082 (G>C) NS NSHylobates vs. Macaca NS NS NS NS NS NSHylobates vs. Cebus NS 0.0870 (H>C) NS NS NS NSCebus vs. Macaca 0.0108 (C<M) 0.0588 (C<M) NS NS NS NS

a P values from M-W U tests. NS, nonsignificant.b Small samples (n<3) preclude the inclusion of Pongo and Pan paniscus in these analyses and Homo are excluded because wehave mean values.c P 5 Pan troglodytes, G 5 Gorilla, H 5 Hylobates syndactylus and H. lar, M 5 Macaca mulatta, C 5 Cebus albifrons and C.capucinus.



difference in absolute masseter PCSA between Gorillaand Cebus is eliminated. Ranges for masseter PCSA forPongo, Gorilla, and P. troglodytes overlap (Fig. 4b).While we do not see statistically significant differences,scale-free ratios are not qualitatively similar across alltaxa, particularly for those samples not included in sta-tistical tests. For example, Homo and Hylobates exhibitcomparatively smaller PCSA0.5/jaw length values com-pared with many other hominoids (Fig. 4b).

Relative fiber length. Relative fiber length (NLf) alsoshows considerable overlap among species (Table 1 andFig. 5). Average masseter NLf is relatively longest in Go-rilla and Homo, with the single P. paniscus individualfalling at the high end of the Gorilla range. Though therange for Pan troglodytes overlaps with Gorilla, chimpaverage masseter fiber lengths are notably relativelyshorter and similar to those observed for Pongo (Fig. 5).By contrast, Homo and P. troglodytes have relativelylong temporalis fibers while temporalis NLf is relativelyreduced in Gorilla. We note that P. troglodytes displayslarge within-species variation for relative temporalisNLf compared with other hominoids (Fig. 5).

Architectural trade-offs between PCSA and fiberlength. The architectural trade-off between relativemasseter PCSA0.5 and NLf (relative maximum excur-sion/contraction velocity) is significant (r 5 20.388,P 5 0.046; Fig. 6). There is no evidence of an architec-tural trade-off for the temporalis (r 5 20.267, P 5 0.283).While individuals with relatively larger PCSAs trend to-ward having relatively shorter fibers, there is appreci-able scatter and little evidence that some ape specieshave evolved toward maximizing relative muscle force at

the expense to relative excursion/contraction velocity (orvice versa). This interpretation is further reinforced bythe absence of a significant inverse relationship whenonly hominoids are analyzed (r 5 20.193, P 5 0.473).

Fig. 4. Box plots depicting from left to right variation in masseter (averages lightly shaded, single specimens and Homo solidthin lines) and temporalis (averages darkly shaded, single specimens and Homo solid thick lines) A) PCSA, and B) PCSA0.5, rela-tive to jaw length. Differences among hominoids in jaw-muscle PCSAs relative to jaw length are diminished with dimensionlessratios and none of the species tested differ significantly (see Table 2). Ratios of PCSAs0.5 adjust for the scale effects of areal relativeto linear dimensions with interspecific size increase. Note that even with dimensionless ratios, H. lar and Homo retain relativelysmall masseter PCSAs while Gorilla retains a relatively large temporalis PCSA among hominoids.

Fig. 5. Box plot depicting from left to right variation inratios of masseter (averages lightly shaded, single specimensand Homo solid thin lines) and temporalis (averages darklyshaded, single specimens and Homo solid thick lines) fiberlength (NLf) relative to jaw length. Hominoids show consider-able overlap in relative jaw-muscle fiber lengths and none ofthe species tested differ significantly (see Table 2).



Scaling of PCSA and NLf. All correlations are signif-icant for PCSA and NLf relative to both jaw length andcondyle-M1 length (P< 0.05), ranging between 0.78 and0.95 for hominoids and 0.86 and 0.93 for our anthropoidsample (Table 3). Across these anthropoids, PCSAs scaleclose to isometry (Fig. 7a) while NLfs trend toward mod-erate positive allometry relative to jaw length (Fig. 7b).However, only the slope for masseter NLf relative to jawlength (b 5 1.353) departs significantly from isometry(F 5 4.887; df 5 1,25; P 5 0.036) (Table 3). By contrast,PCSAs suggest stronger positive allometry in hominoidscompared with anthropoids (Table 3 and Fig. 7a), butslopes for NLf are virtually identical (Fig. 7b) and thereis no statistical support for positively allometric slopesas the large 95% confidence intervals (CIs) do not ruleout isometry (or negative allometry). We observe roughlysimilar scaling patterns relative to condyle-M1 distanceexcept for masseter PCSA which scales with positive al-lometry in the anthropoid sample and stronger positiveallometry in hominoids relative to this load arm esti-mate (Table 3).

DISCUSSION

Jaw-muscle force and mandibular loadresistance in hominoids

Comparative studies of masticatory functional mor-phology are predicated on the assumption that there is apredictable biomechanical relationship among the jawmuscles that help generate external forces, the corre-sponding internal loads on the mandible and thecapacity of the mandible to resist these loads. FollowingHylander (1979a,b), a framework for testing this rela-tionship has been to 1) hypothesize how different feedingbehaviors result in certain movements and in vivo load-ing regimes in representative primates; and 2) test fordifferences in masticatory form as predicted by a biome-chanically efficient morphological solution for a givenmechanical behavior. A biomechanically efficient solutioncould mean that bone is added or shape altered in a way

that counters the increased load but with a minimum ofadditional material.

We took a complimentary approach that extends theseprevious analyses by addressing the relationshipbetween muscle architecture and jaw form in hominoids.We found initial support for a predicted relationshipbetween the relative force-generating capacities of themasseter and relative jaw load resistance ability amonghominoids. This relationship suggests that the capacityof the masseter to generate external forces is related tothe ability of the mandible to counter the loads imposedby these muscles (and other reaction forces). Moreover,this association expands previous analyses linking jaw-muscle activity and in vivo loads in non-hominoid prima-tes (Hylander et al., 1987, 2000; Hylander and Johnson,1994; Vinyard et al., 2007) by suggesting that relativejaw-muscle architecture also relates to variation in man-dibular robusticity. The relationship between musclearchitecture and load resistance ability was only signifi-cant relative to condyle-M1 length as an estimate of theload arm during molar biting (and mastication). Becauseour sample size is small, future work should explore thepotential differences in the relationship between jaw-muscle architecture and mandibular load resistance abil-ity comparing incisal versus masticatory-related scalingfactors.

The relationship between relative masseter PCSA andrelative jaw load-resistance ability in hominoids mayinvolve feeding behavior and diet. For example, the lim-ited food material properties data suggest larger apesingest and chew more resistant foods than smaller apes(Elgart-Berry, 2004; Taylor et al., 2008; Vogel et al.,2008). A potential implication is that with a more resist-ant diet, larger-bodied hominoids may generate rela-tively higher jaw-muscle forces and/or recruit their jawmuscles more frequently, thereby creating larger magni-tude and/or increased number of internal loads in themandible. In turn, these species have a relatively morerobust mandible capable of countering the increased

Fig. 6. Bivariate plot of the relationship between relativemasseter PCSA0.5 versus relative masseter NLf. The absence ofa strong correlation, and the presence of appreciable scatteramong individuals within species, together indicate that anthro-poid primates do not appear to be maximizing muscle force atsome expense to muscle excursion/contraction velocity (or viceversa).

TABLE 3. Reduced major axis slopes (b), 95% confidence inter-vals (CI) for the slopes, y-intercepts, correlation coefficients (r),and sample sizes (n) for bivariate regressions of masseter and

temporalis NLf and PCSAa

b (95% CI) y-Intercept r n

Jaw length vs. all taxaMasseter PCSA 2.057 (1.588–2.224) 27.451 0.927 27Temporalis PCSA 2.128 (1.456–2.405) 27.224 0.907 18Masseter NLf 1.353 (1.024–1.463) 23.422 0.919 27Temporalis NLf 1.425 (0.850–1.612) 23.333 0.864 18

Jaw length vs. hominoids onlyMasseter PCSA 2.698 (1.899–3.085) 210.731 0.924 16Temporalis PCSA 2.599 (1.516–3.347) 29.650 0.936 8Masseter NLf 1.434 (0.742–1.649) 23.840 0.834 16Temporalis NLf 1.868 (0.435–2.604) 25.501 0.814 8

Condyle-M1 length vs. all taxaMasseter PCSA 2.406 (1.055–3.149) 28.193 0.873 9Temporalis PCSA 2.090 (0.894–2.903) 26.346 0.908 7Masseter NLf 1.425 (0.665–1.855) 23.076 0.884 9Temporalis NLf 1.169 (0.521–1.615) 21.778 0.913 7

Condyle-M1 length vs. hominoids onlyMasseter PCSA 3.047 (1.116–4.308) 211.107 0.890 7Temporalis PCSA 2.521 (1.007–3.800) 28.369 0.953 5Masseter NLf 1.386 (0.074–2.080) 22.895 0.777 7Temporalis NLf 1.261 (20.108–2.272) 22.188 0.858 5

a Regressions using condyle-M1 length are based on mean data.



loading. We caution, however, that in addition to thelimited data on food material properties, we lack com-parative in vivo data for any aspect of masticatorystresses in non-human hominoids. Thus, any inferencein hominoids of a functional relationship between jaw-muscle fiber architecture and load resistance ability dur-ing feeding remains tied to inferred loading regimes andcomparative differences in jaw form.

Given our limited knowledge of in vivo loadingregimes, we think it important to point out that our av-erage estimate of mandibular load resistance abilitydoes not represent a specific, biomechanically-efficientsolution (i.e., increased load resistance with a minimumof additional material) to postcanine and incisor loadingregimes experienced during feeding. That having beensaid, we think it provides a reasonable first-orderapproximation of relative differences in the jaw’scapacity to resist loads during biting and chewing. Ourload resistance estimate is based on external linearmeasures and may also track overall jaw size to theextent that shape differences in these load resistancemeasures are correlated with increased size in homi-noids (Ravosa, 2000; Daegling, 2001; Taylor 2002,2006a). In hominoids, there also is a discordancebetween comparative analyses of mandibular load resist-ance abilities based on external linear dimensions (e.g.,Taylor, 2002, 2006a,b) and cortical distribution of bone(e.g. Daegling, 1989, 2001, 2007). A valid concern withexternal linear dimensions in these comparisons is theymay not accurately estimate mandibular biomechanicalproperties, particularly at lower taxonomic levels (Dae-gling, 1989), and external measures cannot account fordifferences in cortical bone distribution that may alterstresses (e.g., Daegling and Hylander, 1998). Given theseconcerns and the size-related changes in hominoid jawshape, the significant correlation between relative mus-cle force production and jaw-load resistance is cautiouslyinterpreted to represent both shape-related rearrange-ments of bone along with the associated changes in over-all mandibular size in hominoids (Daegling, 2002, 2007).

Jaw-muscle structure, function, and scaling inhominoids

Our initial comparative assessment indicates thatmuch of the sampled variation in masseter and tempora-lis PCSA among hominoids is related to size. We basethis conclusion on the fact that while hominoids varysubstantially in absolute jaw-muscle architectural varia-bles (Table 1), simple ratios (e.g., PCSA/jaw length) min-imize the magnitude of these differences (Table 2 andFig. 4a). Scale-free ratios (e.g., PCSA0.5/jaw length) mini-mize these distinctions even further to yield either com-parable architectural proportions among Gorilla, Pan,and Hylobates or significant overlap in proportionsamong species (Table 2 and Fig. 4b).

There are some advantages to being large that relateto intrinsic magnitude and scale. For example, musclePCSA increases as an areal dimension (i.e., as a squarepower) providing a scale effect with size increase relativeto linear dimensions. Thus hominoids, particularly thelarge-bodied apes, may benefit from being big in generat-ing absolutely large muscle forces. It is worth remindingthat conversion of muscle forces into occlusal stressesinvolves molar and incisal contact areas, both of whichchange on a similar areal scale. This means that relativechanges in these two components will partly dictate size-related changes in occlusal stresses generated by differ-ent-sized hominoids. One of the primary, and largelyunknown, factors that will play a key role in determin-ing the benefits of larger size in hominoid feeding is howfood material and structural properties change with sizein the diets of hominoids. Relating structural scaling ofthe masticatory apparatus to size-related changes infood properties and feeding behaviors represents an im-portant area for future research.

Scaling estimates for masseter and temporalis PCSAssuggest positive allometry relative to jaw- and condyle-M1 lengths across hominoids. Anthropoid slopes, how-ever, provide scaling estimates that are close to isometry(Table 3) (see also Anapol et al., 2008). In all cases,

Fig. 7. Bivariate plot for anthropoids (solid line) and hominoids (dashed line) of the relationship between A) Ln masseter PCSAand B) Ln masseter NLf versus jaw length. Masseter PCSA scales close to isometry in anthropoids while hominoids trend towardpositive allometry. Thus, with interspecific size increase, hominoids may be increasing muscle force at a relatively faster rate com-pared with anthropoids. NLf scales with moderate positive allometry in anthropoids and hominoids, suggesting larger taxa maybenefit from relatively greater muscle excursion during ingestive behaviors (see Table 3).



negative allometry and isometry remain possible basedon the 95% CIs. Thus, hominoids appear to differ fromour two anthropoid species by exhibiting a relativelyfaster increase in maximum force-generating potential oftheir jaw adductor muscles with increasing jaw lengths.

When combined with the overall similarity of dimen-sionless ratios for PCSA0.5/jaw length, these differencesin scaling estimates suggest that the larger-bodied homi-noids have jaw-muscle forces that benefited from theincrease in size in comparison to other anthropoids. Inaddition to a range of potential slope values, the smallsamples may limit our ability to identify significant dif-ferences among dimensionless ratios for PCSA0.5/jawlength because of lower statistical power.

Anapol et al. (2008) recently hypothesized that jaw-muscle PCSA should scale with positive allometry asbody size increases. Under the metabolic scaling hypoth-esis, positive allometry of jaw-muscle PCSA would ena-ble larger animals to meet their energetic requirementsby facilitating increased occlusal stresses. Our estimatessuggesting positive allometry of hominoid masseter andtemporalis PCSAs provide support for this metabolicargument. A preliminary analysis of the scaling relation-ship between masseter PCSA and body mass yielded anRMA slope of 0.873 (isometry 5 0.67; r 5 0.813), whilejaw length scales with negative allometry relative tobody mass (RMA slope 5 0.317, r 5 0.892; iso-metry 5 0.33), offering further support for the metabolichypothesis.6 We caution, however, that support for thishypothesis is limited by our small samples and large95% CIs. Future work on larger hominoid samplesshould consider how each of the jaw-adductor musclesscale separately and as a group relative to body size(e.g., Anapol et al., 2008).

Our scaling analyses suggest masseter and temporalisfiber lengths scale with positive allometry in both ourhominoid and anthropoid samples (Table 3 and Fig. 7b).Both Cebus and Macaca fall at the low end of the slopefor masseter NLf, but at comparable jaw lengths theyoverlap with the smaller-bodied Hylobates. The anthro-poid and hominoid slopes also overlap. Collectively, thesepreliminary results do not suggest marked differences inthe relative maximum excursion or contraction velocitiesof the masseter among clades.

The potential positive allometry of fiber length relativeto jaw length may facilitate larger hominoids biting rela-tively large food objects with the anterior teeth by reduc-ing the amount of muscle stretch per degree of angularrotation at the temporomandibular joint. Relatively lon-ger fibers, therefore, could serve to increase range ofmotion (and contraction velocity) without negativelyimpacting force production (Herring and Herring, 1974).This would be functionally advantageous for ingestivebehaviors that involve oral processing with the anteriordentition at relatively wide jaw gapes, as muscle andbite forces diminish when muscle fibers are stretchedbeyond their resting length. This configuration couldbenefit orangutans, for example, who consume larger

and more resistant fruits requiring more extensiveincisal preparation compared with the smaller-bodiedgibbon (Ungar, 1994a,b). We speculate that relativelylong fibers would be advantageous to large-bodied apesengaging in incisal biting even at relatively modest jawgapes, such as chimpanzees who utilize their incisors toprocess fruit (e.g. Lambert, 1999), and orangutans andgorillas for biting on wood (e.g. van Schaik, 2004; Roth-man et al., 2006). One of the benefits of relatively longerfibers for larger hominoids is that it may help offsettheir relatively high temporomandibular joints above theocclusal plane. High jaw joints require more masseterstretch per degree of angular rotation (Herring and Her-ring, 1974). Thus, producing even relatively modest jawgapes may quickly move masseter muscle fibers to oper-ate along the descending limb of the length-tensioncurve, where fibers are stretched and active muscle ten-sion is diminished.

Modern Homo

Modern Homo fall close to the hominoid regressionline for masseter (Fig. 7a) and temporalis (not shown)PCSAs relative to jaw length, similar to some Hylobates,P. troglodytes and Pongo. These findings suggest thathumans have undergone an allometric reduction inmasseter PCSA largely consistent with their attendantdecrease in jaw length. Modern humans retain longmasseter fibers, both absolutely (Table 1) and relative tojaw length (Fig. 7b), similar to some Hylobates, P. panis-cus and Gorilla. In addition, their average masseter pin-nation angle falls well within the observed range forother large-bodied hominoids (Table 1). Thus, any reduc-tion in masseter PCSA relative to jaw length must belargely attributed to a reduction in masseter musclemass. This muscle configuration suggests that modernhumans may have sacrificed absolute masseter muscleforce without appreciably altering muscle excursion orcontraction velocity. Furthermore, if modern humanshave undergone a relative reduction in maximum jawgape, then this reduction is likely attributable to altera-tions in the bony masticatory morphology, rather thanshortening of masseter fibers.

The potential reduction in masseter mass may berelated to prior studies demonstrating that humans failto express the superfast “masticatory myosin” (type IIM)found in other anthropoid primates and nonprimatemammals (Rowlerson et al., 1981; Berg et al., 2001;Schachat and Briggs, 2002). Fibers that express mastica-tory myosin are capable of generating high force at a rel-atively rapid rate, leading some (e.g., Stedman et al.,2004) to suggest that the loss of this isoform in humansmay have resulted in some loss of masticatory muscleforce.

Humans are also distinguished from other hominoidsby their apparent evolutionary shift in PCSA relative tocondyle-M1 length. Here, modern humans have a nota-bly reduced masseter PCSA compared with other homi-noids and exhibit the largest residual falling below thehominoid slope (Fig. 8). When contrasted to the scalingpatterns relative to jaw length, the reduction in relativemasseter PCSA is largely due to an increased condyle-M1 length (i.e., our masticatory load-arm estimate) com-pared with other hominoids. The functional consequenceof this relatively longer condyle-M1 length is that mod-ern humans may have undergone a relative reduction in

6Hominoid body mass data were taken from Smith and Jungers(1997). Body mass data for the modern human sample were takenfrom the CDC advanced data from vital and health statistics (Ogdenet al., 2004). The human jaw muscles were harvested from Caucasianmales and females (average age of 70.5 6 12.8 years) and published in1997. Thus, we averaged mean body mass for non-Hispanic whitemales and females aged 60 years and over from the National HealthExamination Survey 1992–2002.



maximum bite forces that could be used for chewing orbiting at the postcanine dentition.

Several factors related to our human sample couldcontribute to the observed shift in morphospace relativeto condyle-M1 length. First, our use of modern humandata from van Eijden et al. (1997) introduces potentialmethods-related error. Second, our muscle PCSA andload-arm estimates are not from the same human sam-ples and there is considerable variation among humanpopulations in mandibular dimensions, including jawlength (Hrdlicka, 1940). Third, jaw-muscle data are froman elderly Caucasian sample (average age of 70 years)

exhibiting significant natural tooth loss. Tooth loss andage may reduce jaw-muscle cross-sectional areas by upto 22% and 37%, respectively (Newton et al., 1993). Thatsaid, van Eijden’s et al. (1997) cross-sectional estimatesare comparable to those previously reported for rela-tively young subjects (22–46 years of age) with intactdentitions (Weijs and Hillen, 1986). In addition, unusu-ally low estimates of jaw-muscle PCSA may characterizemany of the elderly ape specimens taken from zoos andshould similarly affect comparisons involving jaw- orcondyle-M1 lengths. Future evaluation across humanpopulations should provide additional insight into therelationship between jaw-muscle PCSAs and craniofacialdimensions in our species.

Demes and Creel (1988) were among the first to modelhuman bite forces using cranial proxies of jaw-muscleforce (Walker, 1981; O’Connor et al., 2005; Wroe et al.,2010). They argued that modern humans are distin-guished from their ape and early hominin ancestors bydisplaying a reduction in bite force ability comparedwith other primate species of similar body size. Theyattributed the observed variation among species in biteforces primarily to differences in jaw-muscle forces.

Most recently, Wroe et al. (2010) modeled bite forces inextant apes and modern humans using a finite elementapproach. Their estimates of muscle PCSAs were basedon cranial osteometrics following Demes and Creel(1988) and O’Connor et al. (2005). We compared our av-erage PCSA values for masseter and temporalis to esti-mated PCSAs by Wroe et al. across hominoids (Table 4).Both masseter (r 5 0.86, P 5 0.07; n 5 5) and temporalis(r 5 0.89; P 5 0.11; n 5 4) estimates show moderate corre-lations across hominoids. Despite these correlations,masseter values were underestimated in large-bodiedapes by as much as 67% in gorillas and overestimatedby 14% in humans (Table 4). Because we are only report-ing superficial masseter PCSA, we are likely underesti-mating the divergence between these two estimates inthe large-bodied apes. Temporalis was underestimatedby Wroe et al. (2010) across large-bodied apes by asmuch as 71% in gorillas and underestimated by Demesand Creel (1988) by 30% in humans. These differencesunderscore the difficulty of accurately estimating jaw-muscle fiber architecture parameters from craniometricmeasures (Ant�on, 1999, 2000). Moreover, improvementsin models of fossil hominin and hominoid bite forces may

Fig. 8. Bivariate plot for hominoids of Ln masseter PCSAon Ln condyle-M1 length. Modern humans exhibit the largestresidual about the regression slope, suggesting that comparedwith hominoids, our sample of humans has experienced a rela-tive (non-allometric) reduction in the capacity to generate mass-eter force during biting at the first molar. Note that modernhumans fall close to the hominoid slope for masseter PCSA rela-tive to jaw length (Fig. 7A), suggesting that the relativedecrease in masseter force-generating capacity is largely a func-tion of the scaling relationship between load-arm estimatesrather than a substantial rearrangement of masseter internalarchitecture.

TABLE 4. Comparison of estimates of muscle cross-sectional areas (cm2) separately for males and females.a,b

Demes andCreel (1988) Wroe et al. (2011) Current study

Range of %Difference

Between Currentand Previous

Studies

Masseter M F F M F M FGorilla 17.2 10.8 15.3 31.7 32.6 46 53-67Pan troglodytes 12.2 8.2 13.8 15.2 17.8 20 22-54Pongo pygmaeus 5.9 5.1 10.3 NA 14.9 — 31-66Hylobates lar 3.3 2.3 2.1 1.8 NA 45 —Homo sapiens 5.8 — 5.0 14TemporalisGorilla 21.5 13.5 17.9 NA 47.2 — 71Pan troglodytes 15.2 10.3 15.0 22.3 15.3 32 2-33Hylobates lar 4.1 2.9 3.2 3.9 NA 5 —Homo sapiens 7.3 — 10.4 30

a Wroe et al. (2011) provide data for females only.b Values for H. sapiens are averaged across males and females.



be closely tied to more accurate estimates of jaw-muscleforce thereby supporting the need for additional archi-tectural data on apes and humans.

CONCLUSIONS

We evaluated variation and scaling patterns in homi-noid jaw-muscle architecture and compared hominoidswith representative New- and Old-World monkeys. Ourresults provide empirical support for a functional rela-tionship between the masseter’s ability to generateexternal forces and the mandible’s capacity to resistanceinternal loads. This potential relationship may reflectboth size and shape-related changes in the hominoidfeeding apparatus and may be more closely linked tomasticatory over ingestive performance. Results furtherdemonstrate that variation in jaw-muscle fiber architec-ture among small- and large-bodied apes can be attrib-uted to absolute size differences among taxa andallometry. Our preliminary assessment is that hominoidstrend towards positive allometry of muscle PCSAs, sug-gesting that muscle force may increase at a relativelyfaster rate in hominoids compared with other anthro-poids. In our sample, modern humans have experienceda more rapid decrease in jaw length relative to condyle-M1 length compared with other hominoids. Thus, rela-tive reduction in masseter force-generating capacity inour human sample appears to be a function of the load-arm estimate, rather than marked rearrangement of theinternal muscle architecture. These results underscorethe importance of future studies evaluating the relation-ship between jaw-muscle PCSAs and craniofacial dimen-sions across human populations. The trend towardspositive allometry of jaw-muscle fiber length in anthro-poids and hominoids may be linked to changes in inges-tive behaviors with increasing size. However, functionaland adaptive interpretations of observed allometric pat-terns will be strengthened by additional data on inges-tive and masticatory behaviors for hominoids and thestructural and material properties of the foods they pro-cess. The absence of a strong architectural trade-offbetween relative PCSA and relative NLf, and the appre-ciable scatter among individuals within species, togetherprovide little evidence to suggest species-specific sacrificeof muscle force for muscle excursion/contraction velocity(or vice-versa) in small- and large-bodied apes. Addi-tional data on muscle mechanics are needed to betterunderstand how primates meet the competing demandsfor generating relatively large maximum muscle forcesand excursions, particularly when under pressure tofacilitate both for feeding and/or display behaviors (e.g.Daegling et al., 2011). Finally, our results indicate thatcraniometric estimates of muscle force may be plaguedby large errors and argue for the primacy of architec-tural estimates of muscle force for comparative and insilico studies.

ACKNOWLEDGMENTS

The authors gratefully acknowledge the following indi-viduals and institutions who provided the cadaveric mate-rial used in this study: Carel van Schaik (AnthropologicalInstitute and Museum, Z€urich), Richard W. Thoringtonand Linda Gordon (The National Museum of Natural His-tory, Washington D.C.), Bruce Latimer and Lyman Jellema(Cleveland Museum of Natural History, Ohio), ElizabethCurran (NEPRC), David Begun (Department of Anthropol-ogy, University of Toronto, Canada), Richard Bergl (North

Carolina Zoological Park, Asheboro, NC), and Daniel Lei-berman and Carolyn Eng (Harvard University, Cam-bridge, MA). The authors also thank C. Eng, K. Jones, andJasmine Swaniker for assisting in data collection. Fortraining in phylogenetic comparative methods, ABTthanks the AnthroTree Workshop which is supported byNSF (BCS-0923791) and the National Evolutionary Syn-thesis Center (NSF EF-0905606). The authors also appre-ciate the helpful comments of the Editor, A.E., and twoanonymous reviewers.

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