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The Human Mandible and the Origins of Speech

The Human Mandible and the Origins of Speech Hindawi Publishing Corporation Journal of Anthropology Volume 2012, Article ID 201502, 14 pages doi:10.1155/2012/201502 Research Article David J. Daegling Department of Anthropology, University of Florida, Gainesville, FL 32611-7305, USA Correspondence should be addressed to David J. Daegling, daegling@ufl.edu Received 1 November 2011; Accepted 6 February 2012 Academic Editor: Emiliano Bruner Copyright © 2012 David J. Daegling. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Among the unique traits of human mandibles is the finding of relatively greater utilization of cortical bone with respect to other hominoids. The functional significance of this trait is not plausibly linked to masticatory demands given the diminution of the masticatory musculature in human evolution and the behavioral universal of extraoral food preparation in recent humans. Similarly, the presence of more mandibular bone is not a correlated effect of systemic skeletal robusticity, since gracilization of the skeleton is a feature diagnostic of modern humans. The mandibular symphysis in modern humans is manifested as the chin, and it is here where cortical bone hypertrophy is most pronounced. The potential covariation between the expression of the chin and bone hypertrophy is explored in an attempt to clarify their respective biomechanical roles. Current developments in skeletal biomechanics implicate low magnitude, high frequency strains in bone hypertrophy. The physiology of speech production likely produces strains in mandibular bone of greater frequency and lesser magnitude than those associated with mastication. Consequently, language acquisition plausibly accounts for cortical hypertrophy in modern human mandibles. Its role in the evolution and development of the chin is less clear. 1. Introduction species, its evolutionary and functional significance remain incompletely understood [14, 15]. No consensus exists that there is a diagnostic anatomical Despite the ease with which it can be recognized, the indicator for articulate speech in human evolution. This chin has nevertheless been the focus of considerable debate absence of success cannot be attributed to a lack of effort in as to its essence [16]. A consensus of definition is elusive, identifying suitable candidates [1]. Whether unique aspects and no attempt to resolve it will be made here; instead, the of human hyoid, basicranial, or hypoglossal canal morphol- “chin” in this paper refers to an anterior basal swelling of the ogy indicate the capacity for spoken language is contested mandibular symphysis. In this sense, it “requires” anterior [2–6]. Additionally, the appearance of the human chin has incurvatios for its expression. It is also assumed here that, been suggested to indicate the advent of articulate speech although cortical hypertrophy and the expression of the chin [7–9], but no empirical data provide unambiguous linkage both delineate humans from other extant hominoids, these of the physiology of speech with variation in mandibular features can be considered logically separate in terms of symphyseal morphology [10–13]. their adaptive or evolutionary significance. This assumption The human mandible is morphologically distinct from underlies an analytical strategy where the causes and effects other primates both in terms of its proportions and specific of hypertrophy can be considered independently of the anatomical features [11]. Anterior corpus morphology in expression of the chin. In fact, the features are potentially humans is truly unique among anthropoids, in that the part of a single functional complex. In the discussion that fol- lingual transverse tori and genial pit are absent, and the lows, “symphysis” refers to the midline of the mandible (i.e., labial surface is characterized by a basal swelling (the “chin”) the section transected by the midsagittal plane), “corpus” with several definable features idiosyncratic to human jaws refers to the tooth-bearing portion of the jaw, and “anterior (e.g., trigonum mentale, and incurvatio mandibulae anterior). corpus” is the region of the mandible anterior or rostral to Even though the chin is recognized as diagnostic of our the canines. 2 Journal of Anthropology 2. Cortical Bone Hypertrophy in are required. Whether this translates to a relatively benign stress environment depends on what changes in mandibular the Human Mandible size and shape have occurred. Certainly, the shortened Beyond the chin, another feature of human mandibu- mandible of modern humans predisposes the corpus to lar morphology that distinguishes us from other extant reduced stress in terms of bending alone, and despite the hominoids is the relative amount of cortical bone that is reduction in corpus dimensions modern humans appear utilized in the corpus [17]. Relative to mandibular length, to be remarkably “overdesigned” in the postcanine corpus, human mandibles have relatively more bone throughout the having larger dimensions than needed to maintain stresses corpus than Great Apes (Figure 1). In addition, relative to within a sufficient margin of safety [17]. It is in the anterior subperiosteal area, human mandibles incorporate relatively corpus where humans display the greatest hypertrophy of more bone into the symphyseal region of the anterior corpus cortical bone mass (Figure 5), and since this is where the (Figure 2). difference between ape and human corpus dimensions are The unusually dense packing of bone in the anterior strikingly divergent, this hypertrophy could plausibly be corpus of human jaws does not appear to be explicable as associated with a functional response for reducing masti- an effect of allometric scaling (Figure 3). Whether evaluated catory stresses. This explanation is undermined given that against mandibular length (a general-purpose biomechanical adductor force in humans is probably well below that utilized size proxy owing to its being proportional to bending by Great Apes. That is, humans likely do not produce the moment arms that act during mastication [18–22]) or forces necessary to create mandibular stresses equivalent to total subperiosteal area (Figure 4), recent humans display those in Great Apes given the amount of bone we utilize. more bone than expected given the scaling relationships of Comparative data on muscle force are hard to come by, but hominoids as a whole. Human cortical hypertrophy is thus healthy human subjects may typically produce bite forces in not explicable as the predicted outcome of bone mass in a the range of 350–1235 N [28–32], and theoretical analysis mandible of its particular dimensions. suggests that forces between 700 and 1300 N are possible At least three functional explanations serve as competing [33, 34]. By contrast, gorillas and chimpanzee bite force hypotheses to explain cortical hypertrophy in the modern capability may exceed 1500 N [34], and orangutans are human mandible. These hypotheses are (1) bone mass is probably capable of approaching 2000 N of occlusal force related to shifting masticatory demands in recent human [35]. The higher estimates for humans suggest peak occlusal evolution, (2) bone mass in the mandible is correlated with forces approaching those of chimpanzees but with a more factors influencing cortical bone metabolism systemically, efficient conversion of adductor force into useful bite force. and (3) bone mass is related to the unique human capacity The same craniofacial geometry that leads to this greater for articulate speech. Each of these hypotheses is critically efficiency in humans also reduces the magnitude of bending examined presently. moments acting on the mandible, but whether this implies equivalent or reduced stresses in humans relative to other hominoids depends upon which estimate of bite force is 2.1. Shifting Masticatory Demands. Two important events most reflective of human masticatory behavior. Under an assumption that extraoral food processing is ubiquitous for in human evolution are instrumental to understanding recent changes in masticatory biomechanics. One is that anatomically modern Homo sapiens [26], the theoretically the muscles of mastication became smaller relatively early highest occlusal forces that humans produce are unlikely to be routine. Since adductor forces in humans are reduced in the evolution of Homo, although the cause and timing of this event is disputed [24, 25]. What is likely is that relative to large-bodied hominoids, it is thus reasonable to over the course of human evolution, the ability to produce hypothesize that humans experience relatively low levels of large masticatory forces was compromised. The second event bending stress during mastication [17]. was the advent of extraoral food processing, which today In addition to bending, axial torsion of the corpus is a likely source of stress in human mandibles. The prediction represents a ubiquitous feature of human ecology [26]. A certain effect of this technology, whenever and however it of twisting stress magnitudes, however, is complicated by occurred, is that the production of large occlusal forces the fact that it is difficult to estimate the moment arms in twisting from simple consideration of skull morphology. becomes progressively more unnecessary and less selectively important. Whatever the chain of causality between reduced In absolute terms, torsionalstrengthinhumansisreduced musculature and food processing technology may have relative to Great Apes (Table 1), but when scaled to proxies of available adductor force, Homo wouldappeartoexperience been, the biomechanical effects are straightforward: the genus Homo evolved a masticatory apparatus less capable less stress compared to chimpanzees. Given an assumption of producing largeocclusalforceswithnoapparentcostto that twisting moments in humans are no larger than those in fitness. Great Apes, then it is reasonable to conclude that twisting If one makes the reasonable assumption that the effect, stresses are equivalent, if not lower, in humans relative to apes. if not the intent, of extraoral food processing was to make the bolus less resistant to breakdown (see [27]for While confirmatory data are currently lacking, the pre- explanation of the material parameters involved), then ceding discussion supports the inference that the bending and twisting moments produced by humans do not produce the recent human masticatory environment is relatively benign in terms of the muscular and biting forces that the types of stresses that would account for the amount of Journal of Anthropology 3 0.2 p p g g g 0.15 300 p g g g p p t g p g g g t t t t p p t p 200 t p t g p t 0.1 t hhh h h hh h hh hhhhh hh h Pan Pongo Gorilla Homo 40 60 80 100 120 140 160 180 Figure 1: The ratio of mandibular bone area (mm raised to the 0.5 Mandibular length power) in midsagittal section to mandibular length (mm, measured from infradentale to the intersection of the midsagittal plane with Figure 3: Regression of cortical area in midsagittal section on the gonion-gonion chord)) in samples of adult great apes and mandibular length (r = 0.93) for an adult sample of 100 hominoid humans (N = 10 males and females for each taxon). 25th and mandibles (N = 10 males and females of Pan troglodytes [t],Pongo 75th percentiles (box), median (line), 10th and 90th percentiles pygmaeus [p], Gorilla gorilla [g],Homo [open circles], Hylobates (whiskers) and outliers are shown. For this index, ANOVA is lar and agilis [h]) [23]. The modern human sample (open circles) significant (P < 0.001), and unplanned comparisons show no is superimposed on the hominoid regression. Human mandibles difference among the apes while humans differ from each ape possess more bone than expected based on scaling relationships species at P < 0.05. This finding of significantly greater amount among all hominoids, based on a G-test for the random distribution of bone given jaw length in humans applies throughout the corpus of residuals above and below the regression line (P < 0.001). [17]. 0.8 p g g g 0.6 p 300 p g p g pg g p p g t g p g g t t t t p p t p t p 200 t 0.4 t p hhhhhhh hhh hhhhhhhh 0.2 h 0 200 400 600 800 1000 1200 1400 1600 Pan Pongo Gorilla Homo Subperiosteal area Figure 2: Mandibular bone area (mm ) in midsagittal section as a Figure 4: Regression of cortical area in midsagittal section on fraction of total subperiosteal area in samples of adult great apes subperisoteal area (r = 0.95) for a sample of 100 hominoid and humans (N = 10 males and females for each taxon). 25th mandibles (N = 10 males and females of Pan troglodytes [t],Pongo and 75th percentiles (box), median (line), 10th and 90th percentiles pygmaeus [p], Gorilla gorilla [g],Homo [open circles], Hylobates (whiskers) and outliers are shown. For this index, ANOVA is lar and agilis [h]) [23]. The modern human sample (open circles) significant (P < 0.001), and unplanned comparisons show no is superimposed on the hominoid regression. Human mandibles difference among the apes while humans differ from each ape possess more bone than expected based on scaling relationships species at P < 0.05. This finding of significantly greater bone among all hominoids, based on a G-test for the random distribution packing in humans is most pronounced in the anterior corpus [17]. of residuals above and below the regression line (P < 0.001). bone found in human jaws. Since humans may not expe- The premise of a functional linkage between mandibular rience stress magnitudes equivalent to other anthropoids, bone mass and geometry on the one hand, and masticatory then the hypothesis that cortical hypertrophy in human forces on the other, is merely a specific invocation of the mandibles represents a structural response to masticatory general principle that the developmental loading environ- forces is not compelling. This argument assumes that human ment governs bone modeling [36, 37]. Alterations to bone bone is responsive to mechanical stress in the same manner mass and geometry are the outcome of modeling activity as bone tissue in nonhuman primates. (particularly during growth), while bone remodeling is the 0.5 Cortical area /mandibular length Cortical area/subperiosteal area Cortical area Cortical area 4 Journal of Anthropology stress or strain interval that is “ideal” in that it is the target of metabolic activity. On the other hand, if high- frequency loads, irrespective of magnitude, are associated with increased modeling or remodeling activity, then the metabolic response is less clearly directed to a particular range of stress or strain. There is, however, an abundance of evidence that alteration of load history in terms of frequency, magnitude, or both can engender significant changes in bone mass and/or geometry [41, 45, 46]. It is in this light that comparative differences in bone size and shape are interpreted in a biomechanical framework. In the present context, changes in bone mass (cortical packing) or geometry (the contours of the chin) which have culminated in Figure 5: Cortical bone contours in midline sections of gorilla modern human mandibular morphology are conceptualized (left) and human (right) mandibles. Labial aspect is to the right. as the result of evolutionary changes in patterns of stress. Scale bar is 10 mm. In humans, on average, cortical bone accounts Comparative investigations have assumed that changes in for 49% of the overall area enclosed by the periosteal (outer) relative stress magnitude, rather than frequency, are more boundary of the midline section; in gorillas the average fraction of the total area taken up by cortical bone is about 30%. Because important for explaining the form of the human mandible the overall size of the symphysis is significantly smaller than those [11, 14, 47]. of great apes, the added bone in the human symphysis does not match the absolute strength in great ape mandibles. Scaled to mandibular length (an appropriate biomechanical size proxy), 2.2. Systemic Cortical Robusticity. That bone mass is sensitive humans have on average, relatively stronger symphyses [17]. This to systemic effects of hormonal factors and disease is well does not account for the reduced adductor and biting forces that established. More provocative in the context of human humans produce. Accounting for these factors and the fact that our evolution is that the activity levels that influence certain masticatory demands are reduced due to our practice of extroral regions of the skeleton may produce systemic effects which food processing, human jaws appear to be much stronger than mimic functional adaptation to stress on a local scale. The necessary given the mass and distribution of cortical bone. most explicit articulation of this hypothesis proposes that cranial bone thickness may represent an effect of generalized locomotor or other activity rather than being specifically responsive to one or more cranial functions [48]. In its most Table 1: Torsional strength of hominoid mandibles. distilled form, the hypothesis posits that bone adaptation Taxon Mean Standard error Range T/K ratio to local stress spills over beyond an affected region and produces similar effects throughout the skeleton. Beyond Homo 542 37 292–1072 1.6 Lieberman’s limited experimental data, there is scarce empir- Pan 556 40 314–896 2.4 ical support for this idea, although the absence of support is Pongo 879 68 490–1456 1.1 in some part due to a paucity of experimental designs that Gorilla 1729 102 1198–2808 0.9 specifically evaluate the hypothesis. N = 20 (10 males, 10 females) for each taxon. Means, standard errors and Both Asian Homo erectus and Homo neanderthalensis ranges are for a thin-tube model for torsional strength (K,unitsinmm ), are distinguished from Homo sapiens in terms of skeletal which determines strength as a function of area and minimum wall thickness [17, 44]. Nonparametric ANOVA for mean values of K is significant at robusticity, especially in the cranium, and indeed recent P < 0.001. Post hoc tests reveal that all pairwise comparisons are significant human evolution is associated with skeletal gracilization in with the exception of Homo versus Pan (P > 0.05). The T/K ratio estimates the context of shift in foraging strategy [49]. Diminution torsional shear stress, where T is the applied twisting moment. Since the of the mandible is but one feature of this trend [50, 51]. twisting moment arm is difficult to estimate from skeletal material, the Robusticity can be defined in various ways beyond size, moment arm is assumed constant (1.0, arbitrary units), and the applied force is considered to be the summed estimated forces of the jaw adductors however, including the absolute and relative thickness of the from reference [34]. bones under consideration. In the modern human mandible, the cortical bone is unusually thick by hominoid standards even though corpus size itself is considerably reduced more dominant metabolic activity in adulthood [38]. It is (Figure 5). By this criterion of thick cortices, the modern well established that dynamic rather than static loading is human mandible is “robust” in the same way as, for example, implicated in bone metabolic activity [39]. Some models of Neanderthal long bones. Yet this phenomenon of thick bone modeling emphasize strain magnitude as important mandibular bone is not part of a general skeletal feature [40, 41], while experimental data is accumulating that in modern humans because the remainder of the cranio- implicates strain frequency as an important stimulus for facial skeleton is not characterized by cortical hypertrophy. bone formation [42, 43]. The interaction of these variables Consequently, whatever factors underlie systemic skeletal is also an important consideration. robusticity, the human mandible cannot be explained by If strain magnitude represents the stimulus for bone their effects as the packing of bone in the jaw is atypical of formation or resorption, then conceptually there exists some the remainder of the skeleton. Journal of Anthropology 5 2.3. Bone Mass in the Mandible Relates to Speech. The idea observed [64]. Assuming that the transition between syllables that relatively thick cortical bone in the human mandible involves mandibular movements and altered recruitment could be functionally related to speech is nonintuitive in that of the masticatory, suprahyoid, and Genioglossus muscles, phoneme articulation is a low-stress activity compared to these observed rates may provide a first approximation of the mastication. That is, if mastication of unprepared, uncooked loading frequency of the mandible during spoken language. food among apes does not produce cortical hypertrophy Given this assumption, the loading frequency during speech in their mandibles, why should we expect speaking to be may be from 3–5 times greater than those of mastication. causal in producing thick bone in ours? In fact, activities Mandibular bone strain in mastication or speech is not such as talking have been suggested to be a critical consid- known from human subjects. Theoretical modeling studies eration for understanding the relationship of the functional suggest that the difference in strain magnitude between linkage of physiological activity and bone morphology [52]. mastication and speech may exceed two orders of magnitude Accumulating evidence suggests that high-frequency, low- [65, 66]. The anatomical relationships of the masticatory and amplitude strains strongly influence bone metabolic activity suprahyoid musculature to the maxilla and mandible suggest [42, 52, 53], such that introduction of novel loading regimes that the low-amplitude, high-frequency loads associated with involving low magnitude strains (5 με or below) at high speechwillprimarily affect mandibular rather than maxillary frequencies (∼30 Hz) is sufficient to produce significant bone. There are two reasons to suspect that this is true. First, increases in trabecular density and number, bone volume of the extrinsic tongue muscles, Genioglossus originates on fraction, and bone formation rate. These data suggest strain the mandible, and the others have no direct attachment to frequency has an important role in the determination of the maxilla (Hyoglossus, Styloglossus, and Palatoglossus). bone structure. While most work in this area suggests that Second, the opening and closing movements of the mandible cancellous bone formation is most dramatically affected by involve subtle but measurable changes in the width of the imposition of low-magnitude, high-frequency loads, this mandibular arcade owing to the masticatory muscles acting type of loading regime has produced increases in cortical upon it to the exclusion of the maxilla. The lines of action bone mass in human subjects [54]. of the Masseter and Temporalis include a lateral component, The critical question is whether speech produces the and those of the lateral and medial pterygoids include a kind of loading environment that is conducive to sustained medial component (though their primary actions differ, in bone formation in the human mandible, and if talking is that only Lateral Pterygoid is involved in jaw opening [67]). to be uniquely implicated in bone hypertrophy, the loads These small components produce transverse bending during produced must be distinct from those encountered in mas- jaw opening and closing in nonhuman primates [68]. ticatory activity. Human language does involve utilization If the hypothesis that bone hypertrophy in the human of the muscles of mastication to produce the mandibular mandible is functionally related to speech is true, then it movements involved in speech production [55], but at must explain why this hypertrophy is most pronounced in daily cycle numbers which may routinely exceed those the anterior corpus, whereas the distribution of bone is less associated with feeding. The complex movements of the distinct from other hominoids in the postcanine corpus. tongue required for phoneme production likely involve There are two effects of language use, one local and one continuous activity in suprahyoid muscles with mandibular remote, which can be postulated to explain this. First, both insertions, most notably Genioglossus [56, 57]. Because the Genioglossus and the anterior belly of the Digastric insert mandible is moved without resistance during speaking and on the lingual inferior symphysis: the former muscle is more the glossal musculature is relatively diminutive with respect or less constantly active in speech, and the latter is used for to the mass of the mandible, speech would appear to be positioning the jaw during certain speech tasks [69]. The capable of imposing low-magnitude stresses at relatively high forces exerted by these muscles on the symphyseal bone are frequency. dynamic and low and probably have negligible impact on the Chewing cycle frequency in humans averages about strain field in the postcanine region. Second, the actions of 1.4 Hz [58], with a range of 1.2–1.7 for masticating foods the masticatory muscles in positioning the mandible during of various hardness [59]. Speech rates will obviously be speech tasks will produce small transverse bending moments variable, and one concern is what should count as a speech that will have their largest effects in the anterior rather than “cycle” in the intended biomechanical context. In a study the posterior corpus. contrasting masticatory movements with an artificial speech The preceding points should not be taken to mean task, duration of opening and closing movements was that the biomechanical impact of speech is confined to the significantly lessened in speech [60], supporting the idea anterior corpus. Other muscles important in speech produc- that speech “frequency” is typically greater than masticatory tion (e.g., Mylohyoid) probably have local effects at their frequency. Speech rates have been quantified to 3.5–6.5 insertions, although the overall geometry of the mandible syllables/s [61]) and 6.7 morae/s [62]. From polysyllabic makes it unlikely that anything other than the muscles of English word durations of native and nonnative speakers, mastication produce significant bending or twisting of the rates between 4.5–5.0 syllables/s are observed [63]. Inves- jaw during speech. Any such moments induced in speech tigation of speaking rate over 5,000 utterances (over four will have global effects in the sense that they influence hours of data) suggest similar rates but underscore the the strain field all along the corpus, but these effects will variability intrinsic to conversational speech in that a range not be uniform. One of the most striking features of the of values from over 1 to nearly 10 syllables/second can be human mandible is that given overall size, there is more 6 Journal of Anthropology bone than expected everywhere in the corpus [17]. This is of its size relative to moment arm and force proxies. Because consistent with the observation that the masticatory muscles this type of comparison is necessarily intraspecific, the are intimately involved with speech, because their actions analysis represents an extreme case of narrow allometry, will have stress effects throughout the mandible. Based and high correlations are not expected even if a significant on anatomical relationships and biomechanical principles, bivariate relationship is observed. Figures 6, 7,and 8 relate strains arising from speech activity will likely be highest in chin size to those variables which are expected to covary with the region of the chin—that uniquely human trait which it if mitigation of masticatory stress is important in modern allows us to identify ourselves in the fossil record. This humans. In each case, this covariation is sufficiently tenuous observation then prompts the question of whether the chin that we may reasonably suppose that the relationship is weak itself is related to the acquisition of spoken language. if it exists at all. In the case of significant regression of chin size on bicanine breadth, this does correspond to the idea that coronal bending is the critical load influencing the 3. Revisiting the Chin Problem human anterior corpus [14], but as chin size is explained by a mere 4% of the variance in bicanine breadth, this The idea that the human chin is the product of language apparent relationship may equally plausibly be interpreted as is not new [8, 9], and the hypothesis is still being explored acorrelatedeffect of somatic size [76]. These observations, in today [7]. It is an attractive hypothesis in that it ties together addition to the foregoing point that both force and bending two unique human attributes in a single functional package. moment production are probably highly reduced in recent The evolutionary significance of the chin has been pondered humans, weaken the hypothesis that the human chin is foroveracentury(reviewed in refs.[14, 16]), but the recent primarily a response to altered masticatory biomechanics. literature on the subject is divided among essentially four points of view: (1) the chin represents an adaptation to a novel and unique biomechanical environment [14, 70]; 3.2. The Chin Results from Sexual Selection. The dimorphism (2) the chin is the result of sexual selection [71, 72]; (3) of the human chin continues to fuel speculation that it is the chin is but a structural artifact having no important maintained as an object of sexual selection [71], not an biomechanical function [73]; (4) the chin is a structural unreasonable view considering its sex-specific characteristics response to the physiology of speech [7]. [77]. A critical issue is how variation in the bony form of The cortical hypertrophy of the anterior corpus has no the chin influences its appearance in terms of physiognomy. necessary connection to the presence and form of the chin; That is, the chin may be important in its role in shaping however, it is theoretically possible that the distribution patterns of symmetry in the human face rather than in of bone and the geometry of the region are part of a the details of its configuration [72]. In juxtaposing the single functional complex. It is therefore prudent to evaluate sexual selection hypothesis against the masticatory stress whether by explaining the bone packing that is apparently hypothesis, if the bony conformation of the chin is the result unique to humans, the function (or lack thereof) of the chin of sexual selection to the exclusion of masticatory or other might also be revealed. biomechanical stress, males and females might be expected to display divergent morphologies relative to measures of size and shape. Whether the salience of the bony chin in 3.1. The Chin Results from Masticatory Biomechanical Factors. profile (Figure 9) or its shape and size relative to mandibular I argued previously that the chin was the result of changes size (Figures 10 and 11) is considered, there appears to be in human jaw proportions which lessened the impact of no consistent difference between the sexes in midsagittal wishboning strains but did not mitigate another important section, which is the appropriate perspective in evaluating source of masticatory stress, coronal bending of the anterior biomechanical effects. Similarly, there is no indication that corpus by twisting of the postcanine corpora [14]. The there are significant sex differences in humans with respect validity of this hypothesis had certain predictable outcomes. to bone structural properties [16]. If the chin is the product First, the emergence of the chin in the genus Homo would of sexual selection, it has not resulted in obvious differences be closely tied to changes in jaw size and architecture. in biomechanical performance between males and females, Subsequent investigation has shown that support for this is despite the fact that postadolescent growth of the mandible equivocal [15]. Implicit also is the assumption that having is distinct between males and females [78]. The hypothesis a discernible chin confers a mechanical advantage under of sexual selection, however, does not easily lend itself to the critical load (coronal bending) than a mandible lacking explanations of bone hypertrophy [14]. this feature. The results of recent finite-element modeling studies [74, 75] are in conflict on this point. It is thus unclear whether, once size is controlled, the morphology of 3.3. The Chin Is a Structural Artifact. The chin was featured the chin confers a mechanical advantage over a hypothetical as an example of a nonadaptive character in Gould and “nonchinned” morphology. Certainly, the chin does serve to Lewontin’s [80] critique of adaptationism. In that paper, stiffen the anterior corpus, but whether it must therefore the chin was described as the result of interacting growth represent an adaptation to shifting masticatory demands fields without any necessary functional utility; in essence, remains an open question [74]. a necessary but (in itself) selectively unimportant artifact If the chin is a structural response to masticatory of development. While the possibility cannot be denied, as function, there are predictions that follow in terms of scaling explanation this is unsatisfactory since there is no skeletal Journal of Anthropology 7 300 300 200 200 150 150 20 22 24 26 28 30 32 34 60 65 70 75 80 85 90 95 Jaw length Bicanine breadth Figure 6: Chin size relative to mandibular length for a mix- Figure 8: Chin size (mm ) relative to bicanine breadth (mm) for a sexed sample of adult modern humans from the Tigara (N = mixed-sex sample of adult modern humans from the Tigara (N = 57) andElHesa(N = 51) collections housed at the American 57) and El Hesa (N = 51) collections. Daegling [14] hypothesized Museum of Natural History. Mandibular length (mm) represents a that bicanine breadth would covary positively with chin size as this general biomechanical size proxy, such that if forceful mastication is represented the portion of the anterior corpus loaded in coronal important in determining corpus size, the expectation is for positive bending due to twisting of the postcanine corpora. Regression is correlation between the variables. Regression is nonsignificant (P = significant at P = 0.04; however, r = 0.04, indicating that little 0.12) indicating an absence of such a relationship. Chin size (units of the variation in chin size is explicable by variation in bicanine in mm ) is determined as a simple product of midsagittal height and breadth. chin thickness at the tuber symphyseos; that is, there is no accounting for subperiosteal bone area in these measurements. The Egyptian El Hesa sample dates between 200–400 AD; the Tigara sample derives from Point Hope, Alaska between 1200–1700 AD. M 3.5 3 F M M M F 2.5 M FF M M F F F M F F F F M 300 2 F M M F FF F FF M F F M M M F F M FMM 1.5 M F M F F F M 0.5 M 11 12 13 14 15 16 17 18 19 Chin thickness Figure 9: The depth of the anterior incurvatio of the human chin (units in mm) is contrasted with the thickness of the chin (mm) at the tuber symphyseos in the Tigara sample. Thickness is measured perpendicular to the vertical tangent at the most anterior point 300 400 500 600 700 800 900 of the symphyseal tuber; this measurement will be approximately Temporal fossa size (mm ) parallel to the occlusal plane. Sexing for the sample is based on Costa [79] who employed multiple criteria including features of the Figure 7: Chin size relative to temporal fossa size for a mixed-sex os coxae. A deep incisura generally gives the appearance of a more sample of adult modern humans from the Tigara (N = 57) and salient chin, while chin thickness provides a size measure with no El Hesa (N = 51) collections housed at the American Museum necessary indication of distinctiveness. Interestingly, the different of Natural History. Chin size is determined as a simple product shapes said to differentiate males from females are not reflected of midsagittal height and chin thickness at the tuber symphyseos, by these measures, that is, there is substantial overlap of the sexes. and temporal fossa size is likewise the product of fossa length and Thus, there is no definitive sex difference in shape (as measured breadth. If temporal fossa size is proportional to temporalis cross- here) of the chin in midsagittal section. Nevertheless, regression sectional area, this variable serves as a proxy for adductor force, is significant (P = 0.02), indicating that large chins are also more meaning that positive correlation of chin size and fossa size is salient, in that they are associated with larger anterior incisures. expected if masticatory mechanics are functionally linked to corpus Comparison of sexes by analysis of covariance (ANCOVA) reveals morphology. Regression is nonsignificant (P = 0.50), suggesting a no significant difference between male and female slopes (P = 0.90) lack of functional relationship. or intercepts (P = 0.14). Chin size (mm ) Chin size (mm ) Incisura mandibulae anterior depth Chin size (mm ) 8 Journal of Anthropology 0.52 0.5 M M 200 F F 0.48 F 180 M M M 0.46 F F M M F F F M MF F F 160 M F M 0.44 F F F F M M M M 140 F 0.42 M M F F M F M M F M F M M M M F F F F F F F M M 0.4 M F F F F F 120 F F M F F M F M F M F 0.38 F F F FF 100 F F M 0.36 F F F F 80 0.34 0.32 60 65 70 75 80 85 90 95 65 70 75 80 85 90 95 Jaw length Jaw length Figure 11: Chin size (determined as the product of height and Figure 10: An index of chin breadth/height (“shape”) is contrasted breadth) is positively associated with jaw length (P < 0.001; r = with a measure of jaw size (mandibular length, units in mm) 0.24), with substantial overlap of the sexes in both variables. This for the Tigara sample. Sexing for the sample is based on Costa significant finding is suggestive of a functional relationship, but [79]. Regression is nonsignificant (P = 0.15), indicating that the the correlation is plausibly reflected as a general effect of body general geometry of the human symphysis is insensitive to size. The size dimorphism. Daegling’s [14] model of the masticatory loading female sample range encompasses the male range for shape. Thus, of the chin emphasized coronal bending of the anterior corpus shape differences are not apparent between the sexes in midsagittal due to twisting of the postcanine corpora. Torsion of the corpora, section. Comparison of sexes by analysis of covariance (ANCOVA) however, has no necessary scaling relationship with mandibular reveals no significant difference between male and female slopes length. Alternatively, this relationship could reflect a structural (P = 0.89) or intercepts (P = 0.68). response to wishboning strains [68], although it is not known whether this load occurs in human mastication. Comparison of sexes by analysis of covariance (ANCOVA) reveals no significant feature that cannot be assessed in exactly the same terms; that difference between male and female slopes (P = 0.47) or intercepts is, every morphological feature can be accurately described (P = 0.21). as developmentally determined. The finding of cortical hypertrophy does refocus the issue somewhat: why would a mere artifact be associated with such a heavy metabolic reduction. To some degree, the apparently exceptional investment (assuming the form of the chin and the bone enamel thickness in modern humans can be explained in this beneath it have something to do with one another)? way [82, 83]. If this is the correct interpretation, however, With certain specific considerations, the idea of the form a mechanobiological role for modulation of bone mass is of the chin having nothing much to do with mechanical denied or at least requires an exception in the modern human function is more plausible. Weidenreich [13]offered a com- case. This amounts to special pleading in the absence of pelling, but very simple, explanation for the chin’s salience. specific tests. He noted that modern human incisors are highly reduced relative to earlier hominins or for that matter, hominoids. The human chin is thus the consequence of reduced alveolar 3.4. The Chin and Language. The latest contribution to the support for diminutive teeth. The appearance of the chin, role of language in determining the form of the chin is the therefore, will coincide with incisor root reduction in human finite-element study of Ichim et al. [7]. Noting that their evolution. This explanation by itself fails to explain why previous iterations [75] showed no advantage to the chin for the basal portion of the symphysis protrudes anteriorly; masticatory stress, they argued that in a hypothetical non- that is, its persistence conceivably betrays some functional chinned mandible, the action of Genioglossus muscle at a imperative. Krantz [81] opined that space was at a premium particular orientation produced elevated stresses along the in the modern human oral cavity, essentially arguing that the labial anterior corpus reminiscent of the trigonum mentale basal portion of the mandible could not retract and still leave that typifies many human chins. From this, they suggested sufficient room for the oral viscera. Weidenreich’s position that the appearance of language precipitated the formation is particularly germane to the question of the form of the of the chin. chin and inferences about function, because it underscores As noted above, the small strain magnitudes that are the possibility that the chin itself is the result of separate produced in speech may not disqualify the idea that this functional requirements. activity could influence the distribution of bone tissue. Similarly, there is the possibility that cortical hypertrophy Instead, the real issue with this study is whether the isolated in recent humans is an allometric artifact that requires no action of Genioglossus (and its inferred line of action) biomechanical or adaptive explanation. It simply may be provides a realistic load case for spoken language. As several that bone volume in human mandibles is phylogenetically other muscles are involved, this would seem to be unlikely. conserved, while the overall size of the corpus has undergone More importantly, it is also doubtful that Genioglossus is the Chin “shape” Chin size Journal of Anthropology 9 sole culprit for the chin in light of other data concerning structural (and perhaps functional) complex, depending on the muscle’s function. Acting to protrude the tongue, the one’s definition of the chin. Fukase’s [70]work, however, genioglossus is critical for prevention of tongue relapse which indicates that cortical packing characterizes the basal sym- could obstruct the airway of the oropharynx. Consequently, physis as a whole, and the lingual basal region (i.e., in the the muscle is active during respiration and particularly vicinity of the genial spines) is where cortical bone is thickest. during inspiration in alert humans [84]. During sleep, the Thick cortical bone is not a requirement for the mentum muscle shows more or less continuous activity, elevated dur- osseum. ing inspiration, with the exception of intermittent quiescent activity during REM sleep [85, 86]. Consequently, activity 4. Testing the Speech Hypothesis in the Genioglossus is producing low-level strains in the mandible whether or not speaking is taking place. Despite the One apparent problem with the speech hypothesis is that the uniqueness of their laryngeal space, humans do not appear to load frequencies inferred above for speech are still very low be idiosyncratic in recruiting Genioglossus for maintaining compared to the experimental conditions under which bone respiratory airflow [87, 88]. Frequent and ubiquitous activity tissue responds to low-strain magnitudes (30 Hz). If speech in Genioglossus is thus not particular to humans, even produces load frequencies of over 5 Hz, this is close to the if the activity of this muscle during speech is; therefore, lower bound of bone sensitivity to low-magnitude strains the mechanobiological stimulus of this muscle with respect [42] but well below the ideal frequencies for inducing bone to mandibular bone is probably not sufficiently unique augmentation [92]. There are, however, two considerations in people to suppose that it alone counts for symphyseal that suggest that the physiology of speech could effectively morphology. induce bone formation. First, it may be the result of actions There are additional interpretive problems with Ichim associated with the muscles involved in speech but not et al.’s [7] model. By ignoring the suprahyoid muscles as necessarily those confined to the active production of speech. well as those from the trigeminal and facial somitomeres, Muscle activity occurring during relatively nonvigorous but the loadcase that induces the stress field that they accord ubiquitous events (e.g., in maintaining mandibular “pos- significant is highly unrealistic and unsupported by inde- ture”) is implicated in producing high-frequency (10–50 Hz) pendent data. Recruitment of these other muscles which are but low-amplitude strains that appear to be important in known to function during speech [55, 56, 89] necessarily stimulating bone formation [52, 93]. Since the structural changes the details of the stress field in the anterior corpus. characteristics of human muscles involved in speech differ Determining the accuracy of a modeled stress field is a from their homologues in nonhuman primates [94], then formidable task, but even with such a depiction, relating the effects of these muscles in postural maintenance may the details of stress magnitudes and gradients to the specific be qualitatively distinct. A second consideration is that the details of chin morphology is even more challenging. bone literature is replete with examples of dynamic loads Furthermore, anecdotal observation suggests that the mere of varying magnitudes and frequencies having measurable appearance of the chin has no necessary connection to effects on bone modeling and remodeling. Clearly, the language use, regardless of underlying bony morphology. skeleton can respond to a range of combinations of load Angelman’s syndrome is a developmental disorder in which frequency and magnitude [45]. If bone is sensitive to the severe limitation or absence of spoken language is one interplay of daily loading cycles and average cyclical peak symptom, yet individuals presenting with this syndrome are strains, speech may provide a potent stimulus for bone described as having prominent chins [90]. formation that is unusual among primates. It has been Finally, it should be recognized that the semantics of emphasized that the ability of low strains to engender the “chin problem” do matter for its resolution [16]. If one metabolic response in bone is intimately tied to the number defines the chin by criteria of the tuber symphyseos, tubercula of loading cycles per day [52, 92]. Given the discussion of lateralia, and the incurvatio mandibularis, identifying a frequencies above, the number of loading cycles per day biomechanical milieu which accounts for this constellation owing to speech may be orders of magnitude higher than of features is exceedingly difficult. On the other hand, if one those associated with mastication. While the appropriate accepts the heuristic definition that it is “but a blob of bone” data are lacking, a thought experiment may underscore [11, page 4] then deciding its evolutionary significance is a the plausibility of the speech hypothesis. Assuming a load tidier endeavor, if not more imprecise. Focusing exclusively frequency of 5 Hz, speaking for 5–10 minutes an hour for on the property of bone mass, the mystery of the chin still 16 hours produces 24,000–48,000 loading cycles in a single prevails; it is likely that there is more bone here than we need. day. This range encompasses the 36,000 cycle daily stimulus Our confusion stems from the underlying assumption that that can promote bone activity with strains as small as 5– the goal of bone formation and maintenance is to make sure 10 με [52, 95]. Unresisted opening of the jaws in macaques that bones are exactly as strong as they need to be. Natural creates bending strains of ∼100 με, and licking behaviors selection need not lead to this state of affairs [91]. create strains between 100–300 με [68]. Even granting the What is important to disentangle is whether cortical excessive amount of bone in human jaws, it appears likely hypertrophy itself explains the human chin. If bone hyper- that strains engendered during speech would exceed 5 με. trophy is localized at the labial swelling of the human A desired initial test of the speech hypothesis is the exam- symphysis (tuber symphyseos), then the chin and cortical ination of the assumptions recruited in the above argument. hypertrophy could be reasonably viewed as part of a single That is, how do speech rates and frequencies compare with 10 Journal of Anthropology those of mastication over day-to-day intervals? Modeling the bution in the anterior corpus is relatively meager. Specimens which preserve the symphyseal region (e.g., the SKW 5 actions and activity of all the muscles involved with speech mandible of Paranthropus robustus) may nevertheless not is obviously an involved undertaking, but without such preserve the internal contours of bone very well due to information the nature of loads and the concomitant stresses factors of fossilization [99]. The anterior corpus of SK 15 in the human mandible, the biomechanical effects of speech (the type of “Telanthropus,” likely an early species of Homo)is will remain uncertain. In general terms, the details of bone unlike that of modern humans in terms of geometry (i.e., it deployment in the human mandibular corpus would suggest lacks a discernible chin) but occupies the lower end of the thatspeechproducesstresspatternswhich inducemodeling modern human range in terms of cortical area, relative to and remodeling that are for the most part localized in the both subperiosteal area and mandibular length [23]. Homo anterior corpus. Theoretical or experimental evidence to the floresiensis mandibles are quite unlike modern humans in contrary would undermine the hypothesized relationship. terms of symphyseal morphology and relative corpus size; A second test is developmental: assuming the pattern published CT images do not indicate the modern human of cortical bone distribution is not established in utero or pattern of cortical hypertrophy, at least in the postcanine prior to language acquisition, the adoption of speech may corpus [100]. Neanderthal mandibular remains have been be associated with ontogenetic changes in bone mass in the examined by computed tomography [101, 102], so at least corpus. The weakness of this test, however, is in these initial some data needed to investigate cortical packing in H. assumptions that the general pattern of bone distribution is neanderthalensis are already collected. A finding of cortical developmentally labile in the extreme. There exist data to hypertrophy in mandibles lacking a chin among Pleistocene suggest that this is a na¨ıve premise and that skeletal mass and Homo in association with indications of symbolic behavior geometry are subject to species-specific canalization [96], (e.g., [103]) would suggest that the modern human chin is despite the capacity for bone to change mass and geometry not a diagnostic feature of articulate speech. developmentally. Bone packing in the human symphysis, despite being quantitatively distinct from other primates, is 5. Rethinking Functional Adaptation still highly variable in that the fraction of symphyseal cross- sectional area occupied by cortical bone can range from 32– The distilled version of Wolff ’s Law, that maximation of 72% [17]. Given the difficulties facing us in interpreting strength with a minimum of material is the selective target the relationship of skeletal form to physiological activity of bone metabolic activity, has been rightly criticized in [97], we should be loath to assume that most of this recent years owing to an accumulation of contrary data variance in relative bone thickness is explained primarily [44, 97, 104–106]. The idea that bone morphology represents by whether an individual was verbose or taciturn. Given a structural solution to minimize biomechanical stress is no experimental designs that have uncovered the influence of longer tenable, but what exactly is being optimized in the high-frequency strains to bone metabolism, one hypothesis skeleton is enigmatic [93]. Whether the proposed linkage worth exploring is that the onset of speech activity is of speech to mandibular bone distribution is valid or not, associated with increases in mandibular bone mass. Certainly what seems clear is that bone deployment in the mandible is suckling activity immediately provides a high-frequency, suboptimal with respect to a criterion of obtaining a globally low-magnitude environment in all mammals postnatally, but constant relationship between stress and strength. Perhaps the developmental timing in human speech acquisition is what we are observing is instead a general strategy of bone sufficiently narrow that our discrimination of a temporally adaptation in which the particulars of a loadcase are less specific period of bone hypertrophy should be possible. important that the general dynamic features of a loading regime, such that the metabolic activity of bone is effective The implications of this hypothesis—that articulate but not necessarily economical with respect to structural speech underlies cortical hypertrophy in human mandi- integrity. bles—for paleoanthropological inference are large, but the current absence of supportive data means that its application to the fossil record is largely speculative. There is, however, 6. Conclusions one scenario which itself could provide an important, if not decisive, test. Given that language is a symbolic capacity and High-frequency, low-magnitude loads associated with artic- that some aspects of material culture have unmistakable sym- ulate speech are hypothesized to explain the apparent bolic content, it is reasonable to assume that the presence of paradox of hypertrophied mandibular bone in contrast to symbolic, nonutilitarian artifacts is indicative of the capacity the reduced bone thickness that typifies the remainder for language. The presence of a nonhuman pattern of bone of the modern human skull. Current understanding of distribution in hominin mandibles which are associated bone metabolic activity is consistent with the hypothesis with symbolic artifacts would essentially refute the speech that speech production accounts for the relatively greater hypothesis. Alternatively, provided supportive experimental bone volume that typifies human mandibles in contrast to and developmental data are collected, the observation of nonhuman primates. The detection of elevated bone mass in cortical hypertrophy in the human fossil record could fossil mandibles may thus provide insight into the origins of productively inform questions of the appearance of modern speech in human evolution. human behaviors [98] through inference of language ability. The fact that the greatest concentration of cortical bone Despite the abundance of mandibular remains in the within sections is most apparent in the anterior mandible hominin fossil record, information on cortical bone distri- is consistent with inference of the general effects of jaw Journal of Anthropology 11 loading during speech. Bending moments from the muscles [10] R.H. Biggerstaff, “The biology of the human chin,” in OrofacialGrowthand Development,A.ADahlberg andT.M. of mastication will be largest in midsagittal section and Graber, Eds., pp. 71–87, Mouton, Paris, France, 1977. Geniohyoid, Genioglossus and Anterior Digastric muscles, [11] E.L. DuBrul and H. Sicher, The Adaptive Chin,Charles C. which are intimately involved in speech production, directly Thomas, Springfield, Ill, USA, 1954. attach in this region as well. [12] T. T. Waterman, “The evolution of the chin,” American This hypothesis is testable by different means, but at Naturalist, vol. 50, pp. 237–242, 1916. present it is not directly supported by experimental, devel- [13] F. Weidenreich, “The mandibles of Sinanthropus pekinensis: opmental or comparative data. Instead, the observations a comparative study,” Palaeontologica Sinica Series D, vol. 7, on bone mass in human mandibles are merely consistent pp. 1–164, 1936. with the idea that the mechanobiology of speech can effect [14] D. J. Daegling, “Functional morphology of the human chin,” bone formation to a significant degree. In addition, whether Evolutionary Anthropology Issues, News, and Reviews, vol. 1, bone hypertrophy is functionally linked to the evolutionary no. 5, pp. 170–177, 1993. appearance of the chin remains an open, and to some degree [15] S. D. Dobson and E. Trinkaus, “Cross-sectional geometry and separate, question. morphology of the mandibular symphysis in Middle and Late Pleistocene Homo,” Journal of Human Evolution, vol. 43, no. 1, pp. 67–87, 2002. Acknowledgments [16] J. H. Schwartz and I. Tattersall, “The human chin revisited: what is it and who has it?” Journal of Human Evolution, vol. Data collected for this project was supported in part by 38, no. 3, pp. 367–409, 2000. NSF (BNS 8920592 and BCS 0922429) and by an American [17] D. J. Daegling, “Relationship of bone utilization and biome- Museum of Natural History Collection Study grant to the chanical competence in hominoid mandibles,” Archives of author in 1992. The author also wishes to thank Ian Tattersall Oral Biology, vol. 52, no. 1, pp. 51–63, 2007. and Gary Sawyer for their support and assistance during my [18] W. L. Hylander, “Mandibular function and biomechanical stay at the museum. K. Kupczik and an anonymous reviewer stress and scaling,” Integrative and Comparative Biology, vol. provided helpful critique and commentary on a previous 25, no. 2, pp. 315–330, 1985. draft. [19] M. J. Ravosa, “Jaw morphology and function in living andfossilOld Worldmonkeys,” International Journal of Primatology, vol. 17, no. 6, pp. 909–932, 1996. References [20] M. J. Ravosa, “Size and scaling in the mandible of living and [1] W. L. Jungers, A. A. Pokempner, R. F. Kay, and M. Cartmill, extinct apes,” Folia Primatologica, vol. 71, no. 5, pp. 305–322, “Hypoglossal Canal Size in Living Hominoids and the Evolution of Human Speech,” Human Biology, vol. 75, no. 4, [21] M. Bouvier, “Biomechanical scaling of mandibular dimen- pp. 473–484, 2003. sions in New World Monkeys,” International Journal of [2] B.Arensburg,L.A.Schepartz,A.M.Tillier,B.Vandermeer- Primatology, vol. 7, no. 6, pp. 551–567, 1986. sch, and Y. Rak, “A reappraisal of the anatomical basis for [22] M. J. Ravosa, “Structural allometry of the prosimian speech in middle Palaeolithic hominids,” American Journal of mandibular corpus and symphysis,” Journal of Human Evo- Physical Anthropology, vol. 83, no. 2, pp. 137–146, 1990. lution, vol. 20, no. 1, pp. 3–20, 1991. [3] D.Degusta,W.H.Gilbert,and S. P. Turner,“Hypoglossal [23] D.J. Daegling, Geometry and biomechanics of hominoid canal size and hominid speech,” Proceedings of the National mandibles, Ph.D. dissertation, State University of New York, Academy of Sciences of the United States of America, vol. 96, Stony Brook, NY, USA, 1990. no. 4, pp. 1800–1804, 1999. [24] M. A. McCollum,C.C.Sherwood,C.J.Vinyard,C.O.Love- [4] R.F.Kay,M.Cartmill, andM.Balow,“Thehypoglossalcanal joy, and F. Schachat, “Of muscle-bound crania and human and the origin of human vocal behavior,” Proceedings of the brain evolution: the story behind the MYH16 headlines,” National Academy of Sciences of the United States of America, Journal of Human Evolution, vol. 50, no. 2, pp. 232–236, 2006. vol. 95, no. 9, pp. 5417–5419, 1998. [25] H. H. Stedman, B. W. Kozyak, A. Nelson et al., “Myosin gene [5] J. T. Laitman and R. C. Heimbuch, “The basicranium of Plio- mutation correlates with anatomical changes in the human Pleistocene hominids as an indicator of their upper respira- lineage,” Nature, vol. 428, no. 6981, pp. 415–418, 2004. tory systems,” American Journal of Physical Anthropology, vol. [26] R. Wrangham and N. Conklin-Brittain, “Cooking as a 59, no. 3, pp. 323–343, 1982. biological trait,” Comparative Biochemistry and Physiology A, [6] P. Lieberman, J. T. Laitman, J. S. Reidenberg, K. Landahl, and vol. 136, no. 1, pp. 35–46, 2003. P. J. Gannon, “Folk psychology and talking hyoids,” Nature, [27] K. R. Agrawal, P. W. Lucas, J. F. Prinz, and I. C. Bruce, vol. 342, no. 6249, pp. 486–487, 1989. “Mechanical properties of foods responsible for resisting [7] I. Ichim, J. Kieser, and M. Swain, “Tongue contractions food breakdown in the human mouth,” Archives of Oral during speech may have led to the development of the Biology, vol. 42, no. 1, pp. 1–9, 1997. bony geometry of the chin following the evolution of [28] L. M. Waugh, “Influence of diet on the jaw and face human language: a mechanobiological hypothesis for the of the American Eskimo,” Journal of the American Dental development of the human chin,” Medical Hypotheses, vol. 69, Association, vol. 24, pp. 1640–1647, 1937. no. 1, pp. 20–24, 2007. [29] E. Helkimo, G. E. Carlsson, and M. Helkimo, “Bite force and [8] A. Keith, Antiquity of Man, Williams and Norgate, London, state of dentition,” Acta Odontologica Scandinavica, vol. 35, UK, 1916. no. 6, pp. 297–303, 1977. [9] O. Walkhoff, “Die menschliche Sprache in ihrer Bedeutung [30] G. J. Pruim,H.J.deJongh,and J. J. TenBosch,“Forces acting fur die funktionelle Gestalt des Unterkiefers,” Anatomischer on the mandible during bilateral static bite at different bite Anzeiger, vol. 24, p. 129, 1904. 12 Journal of Anthropology force levels,” Journal of Biomechanics, vol. 13, no. 9, pp. 755– [48] D. E. Lieberman, “How and why humans grow thin skulls: 763, 1980. experimental evidence for systemic cortical robusticity,” American Journal of Physical Anthropology, vol. 101, no. 2, pp. [31] D. P. Sinn, E. A. de Assis, and G. S. Throckmorton, “Mandibular excursions and maximum bite forces in patients 217–236, 1996. with temporomandibular joint disorders,” Journal of Oral [49] C. S. Larsen, Bioarchaeology: Interpreting Behavior from the and Maxillofacial Surgery, vol. 54, no. 6, pp. 671–679, 1996. Human Skeleton, Cambridge University Press, Cambridge, [32] M. C. Raadsheer, T. M. G. J. van Eijden, F. C. van Ginkel, UK, 1997. and B. Prahl-Andersen, “Contribution of jaw muscle size and [50] D. C. M. Boyd, A Functional Model for Masticatory-Related craniofacial morphology to human bite force magnitude,” Mandibular, Dental, and Craniofacial Microevolutionary Journal of Dental Research, vol. 78, no. 1, pp. 31–42, 1999. Change Derived from a Selected Southeastern Indian Skeletal Temporal Series, University of Tennessee, Knoxville, Tenn, [33] B. Demes and N. Creel, “Bite force, diet, and cranial morphology of fossil hominids,” Journal of Human Evolution, USA, 1988. vol. 17, no. 7, pp. 657–670, 1988. [51] C. S. Larsen, “The anthropology of St. Catherine’s Islandpp. [34] S. Wroe,T.L.Ferrara,C.R.McHenry,D.Curnoe, and 3. prehistoric human biological adaptation,” Anthropological Papers of the American Museum of Natural History, vol. 57, U. Chamoli, “The craniomandibular mechanics of being human,” Proceedings of the Royal Society B, vol. 277, no. 1700, no. 3, pp. 155–276, 1982. pp. 3579–3586, 2010. [52] C. Rubin, A. S. Turner, C. Mallinckrodt, C. Jerome, K. Mcleod, and S. Bain, “Mechanical strain, induced noninva- [35] P. W. Lucas, C. R. Peters, and S. R. Arrandale, “Seed-breaking forces exerted by orang-utans with their teeth in captivity and sively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone,” Bone, vol. 30, no. 3, pp. 445–452, a new technique for estimating forces produced in the wild,” American JournalofPhysicalAnthropology,vol. 94, no.3,pp. 2002. 365–378, 1994. [53] C. Rubin, A. S. Turner, S. Bain, C. Mallinckrodt, and K. McLeod, “Low mechanical signals strengthen long bones,” [36] D. R. Carter and G. S. Beaupre, Skeletal Function and Form, Cambridge University Press, Cambridge, UK, 2001. Nature, vol. 412, no. 6847, pp. 603–604, 2001. [37] L. E. Lanyon and C. T. Rubin, “Functional adaptation in [54] V. Gilsanz, T. A. L. Wren, M. Sanchez, F. Dorey, S. Judex, skeletal structures,” in Functional Vertebrate Morphology,M. and C. Rubin, “Low-level, high-frequency mechanical signals enhance musculoskeletal development of young women with Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake, Eds., pp. 1–25, Harvard University Press, Cambridge, Mass, USA, low BMD,” Journal of Bone and Mineral Research, vol. 21, no. 9, pp. 1464–1474, 2006. [55] J. W. Folkins, “Muscle activity for jaw closing during speech,” [38] R. B. Martin, D. B. Burr, and N. A. Sharkey, Skeletal Tissue Mechanics, Springer, New York, NY, USA, 1998. Journal of Speech and Hearing Research, vol. 24, no. 4, pp. 601–615, 1981. [39] L. E. Lanyon and C. T. Rubin, “Static vs dynamic loads as an [56] K. M. Hiiemae and J. B. Palmer, “Tongue movements in influence on bone remodelling,” Journal of Biomechanics, vol. 17, no. 12, pp. 897–905, 1984. feeding and speech,” Critical Reviews in Oral Biology and Medicine, vol. 14, no. 6, pp. 413–429, 2003. [40] H. M. Frost, “Bone “mass” and the “mechanostat”: a [57] M. Kumada,R.T.Todd, F. Bell-Berti,M.Niitsu,H.Hirose, proposal,” Anatomical Record, vol. 219, no. 1, pp. 1–9, 1987. and S. Niimi, “Functions of the muscles of the tongue during [41] C. T. Rubin and L. E. Lanyon, “Regulation of bone mass by speech,” Journal of the Acoustical Society of America, vol. 104, mechanical strain magnitude,” Calcified Tissue International, no. 3, pp. 1819–1820, 1998. vol. 37, no. 4, pp. 411–417, 1985. [58] C. F. Ross, D. A. Reed, R. L. Washington, A. Eckhardt, F. [42] C. T. Rubin, K. J. McLeod,T.S.Gross, andH.J.Donahue, Anapol, and N. Shahnoor, “Scaling of chew cycle duration “Physical stimulus as potent determinants of bone morphol- in primates,” American Journal of Physical Anthropology, vol. ogy,” in Bone Biodynamics in Orthodontic and Orthopedic 138, no. 1, pp. 30–44, 2009. Treatment,D.S.Carlson andS.A.Goldstein, Eds.,pp. 75– 91, University of Michigan Center for Human Growth and [59] C. Lassauzay, M. A. Peyron, E. Albuisson, E. Dransfield, and A. Woda, “Variability of the masticatory process during Development, Ann Arbor, Mich, USA, 1991. chewing of elastic model foods,” European Journal of Oral [43] Y. F. Hsieh and C. H. Turner, “Effects of loading frequency on Sciences, vol. 108, no. 6, pp. 484–492, 2000. mechanically induced bone formation,” Journal of Bone and [60] D. J. Ostry and J. R. Flanagan, “Human jaw movement in Mineral Research, vol. 16, no. 5, pp. 918–924, 2001. mastication and speech,” Archives of Oral Biology, vol. 34, no. [44] D. J. Daegling, “The relationship of in vivo bone strain 9, pp. 685–693, 1989. to mandibular corpus morphology in Macaca fascicularis,” [61] E. Fosler-Lussier and N. Morgan, “Effects of speaking rate Journal of Human Evolution, vol. 25, no. 4, pp. 247–269, 1993. and word frequency on pronunciations in conversational [45] D. M. Cullen, R. T. Smith, and M. P. Akhter, “Bone-loading speech,” Speech Communication, vol. 29, no. 2, pp. 137–158, response varies with strain magnitude and cycle number,” Journal of Applied Physiology, vol. 91, no. 5, pp. 1971–1976, [62] H. Kuwabara, “Acoustic and perceptual properties of phonemes in continuous speech as a function of speaking [46] M. R. Forwood and C. H. Turner, “The response of rat tibiae rate,” in Proceedings of the 5th European Conference on Speech to incremental bouts of mechanical loading: a quantum Communication and Technology (EUROSPEECH ’97 ),pp. concept for bone formation,” Bone, vol. 15, no. 6, pp. 603– 1003–1006, Rhodes, Greece, 1997. 609, 1994. [63] M. A. Levent and H. L. H. John, “A study of temporal features [47] J. E. A. Wolff, “A theoretical approach to solve the chin and frequency characteristics in American English foreign problem,” in Food Acquisition and Processing in Primates,D.J. accent,” Journal of the Acoustical Society of America, vol. 102, Chivers, B. A. Wood, and A. Bilsborough, Eds., pp. 391–405, no. 1, pp. 28–40, 1997. Plenum Press, New York, NY, USA, 1984. Journal of Anthropology 13 [64] N. Morgan and E. Fosler-Lussier, “Combining multiple modern human molars,” Journal of Human Evolution, vol. 55, estimators of speaking rate,” Acoustics, Speech and Signal no. 1, pp. 12–23, 2008. Processing, vol. 2, pp. 729–732, 1998. [83] K. Kupczik and J. J. Hublin, “Mandibular molar root [65] T. W. P. Korioth, D. P. Romilly, and A. G. Hannam, “Three- morphology in Neanderthals and Late Pleistocene and recent dimensional finite element stress analysis of the dentate Homo sapiens,” Journal of Human Evolution,vol. 59, no.5,pp. human mandible,” American Journal of Physical Anthropol- 525–541, 2010. ogy, vol. 88, no. 1, pp. 69–96, 1992. [84] E. K. Sauerland and S. P. Mitchell, “Electromyographic [66] M. Motoyoshi, Y. Hama, E. Sugi, K. Takahashi, K. Kamijo, activity of the human Genioglossus muscle in response to and S. Namura, “A finite element model of the human face. respiration and to positional changes of the head,” Bulletin of Stress distribution around the chin due to articulation of the Los Angeles neurological societies, vol. 35, no. 2, pp. 69–73, the five vowels in Japanese,” The Journal of Nihon University School of Dentistry, vol. 38, no. 1, pp. 11–20, 1996. [85] R. C. Basner, J. Ringler, R. M. Schwartzstein, S. E. Weinberger, [67] J. T. Stern Jr., Essentials of Gross Anatomy, FA Davis, and J. Woodrow Weiss, “Phasic electromyographic activity Philadelphia, Pa, USA, 1988. of the genioglossus increases in normals during slow-wave [68] W. L. Hylander, “Stress and strain in the mandibular sleep,” Respiration Physiology, vol. 83, no. 2, pp. 189–200, symphysis of primates: a test of competing hypotheses,” American JournalofPhysicalAnthropology,vol. 64, no.1,pp. [86] E. K. Sauerland and R. M. Harper, “The human tongue 1–46, 1984. during sleep: electromyographic activity of the genioglossus [69] B. Tuller, K. S. Harris, and B. Gross, “Electromyographic muscle,” Experimental Neurology, vol. 51, no. 1, pp. 160–170, study of the jaw muscles during speech,” Journal of Phonetics, vol. 9, pp. 175–188, 1981. [87] R. T. Brouillette and B. T. Thach, “Control of genioglossus [70] H. Fukase, “Functional significance of bone distribution in muscle inspiratory activity,” Journal of Applied Physiology the human mandibular symphysis,” Anthropological Science, Respiratory Environmental and Exercise Physiology, vol. 49, vol. 115, no. 1, pp. 55–62, 2007. no. 5, pp. 801–808, 1980. [71] N. Barber, “The evolutionary psychology of physical attrac- [88] R. F. Fregosi and D. D. Fuller, “Respiratory-related control of tiveness: sexual selection and human morphology,” Ethology extrinsic tongue muscle activity,” Respiration Physiology, vol. and Sociobiology, vol. 16, no. 5, pp. 395–424, 1995. 110, no. 2-3, pp. 295–306, 1997. [72] K. Grammer and R. Thornhill, “Human (Homo sapiens) [89] S. M. Farret, M. Vitti, and M. M. B. Farret, “Electromyo- facial attractiveness and sexual selection: the role of symme- graphic analysis of the mentalis and depressor labii inferior try and averageness,” Journal of Comparative Psychology, vol. muscles in the production of speech,” Electromyography and 108, no. 3, pp. 233–242, 1994. Clinical Neurophysiology, vol. 22, no. 1-2, pp. 137–148, 1982. [73] D. E. Lieberman, “Testing hypotheses about recent human [90] J. Clayton-Smith and L. Laan, “Angelman syndrome: a evolution from skulls: integrating morphology, function, review of the clinical and genetic aspects,” Journal of Medical development, and phylogeny,” Current Anthropology, vol. 36, Genetics, vol. 40, no. 2, pp. 87–95, 2003. no. 2, pp. 159–197, 1995. [91] N. C. Nowlan and P. J. Prendergast, “Evolution of [74] F. Groning ¨ , J. Liu, M. J. Fagan, and P. O’Higgins, “Why do mechanoregulation of bone growth will lead to non-optimal humans have chins? Testing the mechanical signficance of bone phenotypes,” Journal of Theoretical Biology, vol. 235, no. modern human symphyseal morphology with finite element 3, pp. 408–418, 2005. analysis,” American Journal of Physical Anthropology, vol. 144, [92] C. T. Rubin and K. J. McLeod, “Biologic modulation of pp. 593–606, 2011. mechanical influences in bone remodeling,” in Biomechanics [75] I. Ichim, M. Swain, and J. A. Kieser, “Mandibular biomechan- of Diarthrodial Joints,V.C.Mow,A.Ratcliff, and S. L.-Y. Woo, ics and development of the human chin,” Journal of Dental Eds., pp. 97–118, Springer, New York, NY, USA, 1990. Research, vol. 85, no. 7, pp. 638–642, 2006. [93] C. T. Rubin, K. J. McLeod, and S. D. Bain, “Functional strains [76] R. J. Smith, “Categories of allometry: body size versus and cortical bone adaptation: epigenetic assurance of skeletal biomechanics,” Journal of Human Evolution, vol. 24, no. 3, integrity,” Journal of Biomechanics, vol. 23, supplement 1, pp. pp. 173–182, 1993. 43–54, 1990. [77] W. M. Bass, Human Osteology: A Laboratory and Field [94] R. D. Kent, “The uniqueness of speech among motor Manual, Missouri Archaeological Society, Columbia, Mo, systems,” Clinical Linguistics and Phonetics, vol. 18, no. 6–8, USA, 3rd edition, 1987. pp. 495–505, 2004. [78] M. Coquerelle,F.L.Bookstein, andJ.Braga et al., “Sexual [95] C. Rubin, S. Judex, and Y. X. Qin, “Low-level mechanical dimorphism of the human mandible and its association signals and their potential as a non-pharmacological inter- with dental development,” American Journal of Physical vention for osteoporosis,” Age and Ageing,vol. 35, no.2,pp. Anthropology, vol. 145, no. 2, pp. 192–202, 2011. ii32–ii36, 2006. [79] R. L. Costa, Dental pathology and related factors in archaeolog- ical eskimo samples from point hope and Kodiak Island, Alaska, [96] T. M. Cole, “Postnatal heterochrony of the masticatory apparatus in Cebus apella and Cebus albifrons,” Journal of Ph.D. dissertation, University of Pennsylvania, 1977. [80] S. J. Gould and R. C. Lewontin, “The spandrels of San Marco Human Evolution, vol. 23, no. 3, pp. 253–282, 1992. and the Panglossian paradigm: a critique of the adaptationist [97] O. M. Pearson and D. E. Lieberman, “The aging of Wolff ’s programme,” Proceedings of the Royal Society of London B, vol. “law”: ontogeny and responses to mechanical loading in 205, no. 1161, pp. 581–598, 1979. cortical bone,” American Journal of Physical Anthropology, [81] G. S. Krantz, “Sapienization and speech,” Current Anthropol- vol. 39, pp. 63–99, 2004. ogy, vol. 21, no. 6, pp. 773–792, 1980. [98] S. McBrearty and A. S. Brooks, “The revolution that wasn’t: a [82] A. J. Olejniczak, T. M. Smith, R. N. M. Feeney et al., “Dental new interpretation of the origin of modern human behavior,” tissue proportions and enamel thickness in Neandertal and Journal of Human Evolution, vol. 39, no. 5, pp. 453–563, 2000. 14 Journal of Anthropology [99] F. E. Grine and D. J. Daegling, “New mandible of Paranthro- pus robustus from Member 1, Swartkrans Formation, South Africa,” Journal of Human Evolution, vol. 24, no. 4, pp. 319– 333, 1993. [100] P. Brown and T. Maeda, “Liang Bua Homo floresiensis mandibles and mandibular teeth: a contribution to the comparative morphology of a new hominin species,” Journal of Human Evolution, vol. 57, no. 5, pp. 571–596, 2009. [101] J. L. Thompson and B. Illerhaus, “A new reconstruction of the Le Moustier 1 skull and investigation of internal structures using 3-D μCT data,” Journal of Human Evolution, vol. 35, no. 6, pp. 647–665, 1998. [102] P. Bayle, J. Braga, A. Mazurier, and R. Macchiarelli, “Dental developmental pattern of the Neanderthal child from Roc de Marsal: a high-resolution 3D analysis,” Journal of Human Evolution, vol. 56, no. 1, pp. 66–75, 2009. [103] J. Zilhau, D. E. Angelucci, E. Badal-Garcia et al., “Symbolic use of marine shells and mineral pigments by Iberian Nean- derthals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 3, pp. 1023–1028, [104] B. Demes, J. T. Stern Jr., M. R. Hausman, S. G. Larson, K. J. Mcleod, and C. T. Rubin, “Patterns of strain in the macaque ulna during functional activity,” American Journal of Physical Anthropology, vol. 106, no. 1, pp. 87–100, 1998. [105] B. Demes, Y. X. Qin, J. T. Stern Jr., S. G. Larson, and C. T. Rubin, “Patterns of strain in the macaque tibia during functional activity,” American Journal of Physical Anthropology, vol. 116, no. 4, pp. 257–265, 2001. [106] D. E. Lieberman, J. D. Polk, and B. Demes, “Predicting Long Bone Loading from Cross-Sectional Geometry,” American Journal of Physical Anthropology, vol. 123, no. 2, pp. 156–171, 2004. 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The Human Mandible and the Origins of Speech

Journal of Anthropology , Volume 2012 – May 29, 2012

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Copyright © 2012 David J. Daegling. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2090-4045
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10.1155/2012/201502
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Abstract

Hindawi Publishing Corporation Journal of Anthropology Volume 2012, Article ID 201502, 14 pages doi:10.1155/2012/201502 Research Article David J. Daegling Department of Anthropology, University of Florida, Gainesville, FL 32611-7305, USA Correspondence should be addressed to David J. Daegling, daegling@ufl.edu Received 1 November 2011; Accepted 6 February 2012 Academic Editor: Emiliano Bruner Copyright © 2012 David J. Daegling. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Among the unique traits of human mandibles is the finding of relatively greater utilization of cortical bone with respect to other hominoids. The functional significance of this trait is not plausibly linked to masticatory demands given the diminution of the masticatory musculature in human evolution and the behavioral universal of extraoral food preparation in recent humans. Similarly, the presence of more mandibular bone is not a correlated effect of systemic skeletal robusticity, since gracilization of the skeleton is a feature diagnostic of modern humans. The mandibular symphysis in modern humans is manifested as the chin, and it is here where cortical bone hypertrophy is most pronounced. The potential covariation between the expression of the chin and bone hypertrophy is explored in an attempt to clarify their respective biomechanical roles. Current developments in skeletal biomechanics implicate low magnitude, high frequency strains in bone hypertrophy. The physiology of speech production likely produces strains in mandibular bone of greater frequency and lesser magnitude than those associated with mastication. Consequently, language acquisition plausibly accounts for cortical hypertrophy in modern human mandibles. Its role in the evolution and development of the chin is less clear. 1. Introduction species, its evolutionary and functional significance remain incompletely understood [14, 15]. No consensus exists that there is a diagnostic anatomical Despite the ease with which it can be recognized, the indicator for articulate speech in human evolution. This chin has nevertheless been the focus of considerable debate absence of success cannot be attributed to a lack of effort in as to its essence [16]. A consensus of definition is elusive, identifying suitable candidates [1]. Whether unique aspects and no attempt to resolve it will be made here; instead, the of human hyoid, basicranial, or hypoglossal canal morphol- “chin” in this paper refers to an anterior basal swelling of the ogy indicate the capacity for spoken language is contested mandibular symphysis. In this sense, it “requires” anterior [2–6]. Additionally, the appearance of the human chin has incurvatios for its expression. It is also assumed here that, been suggested to indicate the advent of articulate speech although cortical hypertrophy and the expression of the chin [7–9], but no empirical data provide unambiguous linkage both delineate humans from other extant hominoids, these of the physiology of speech with variation in mandibular features can be considered logically separate in terms of symphyseal morphology [10–13]. their adaptive or evolutionary significance. This assumption The human mandible is morphologically distinct from underlies an analytical strategy where the causes and effects other primates both in terms of its proportions and specific of hypertrophy can be considered independently of the anatomical features [11]. Anterior corpus morphology in expression of the chin. In fact, the features are potentially humans is truly unique among anthropoids, in that the part of a single functional complex. In the discussion that fol- lingual transverse tori and genial pit are absent, and the lows, “symphysis” refers to the midline of the mandible (i.e., labial surface is characterized by a basal swelling (the “chin”) the section transected by the midsagittal plane), “corpus” with several definable features idiosyncratic to human jaws refers to the tooth-bearing portion of the jaw, and “anterior (e.g., trigonum mentale, and incurvatio mandibulae anterior). corpus” is the region of the mandible anterior or rostral to Even though the chin is recognized as diagnostic of our the canines. 2 Journal of Anthropology 2. Cortical Bone Hypertrophy in are required. Whether this translates to a relatively benign stress environment depends on what changes in mandibular the Human Mandible size and shape have occurred. Certainly, the shortened Beyond the chin, another feature of human mandibu- mandible of modern humans predisposes the corpus to lar morphology that distinguishes us from other extant reduced stress in terms of bending alone, and despite the hominoids is the relative amount of cortical bone that is reduction in corpus dimensions modern humans appear utilized in the corpus [17]. Relative to mandibular length, to be remarkably “overdesigned” in the postcanine corpus, human mandibles have relatively more bone throughout the having larger dimensions than needed to maintain stresses corpus than Great Apes (Figure 1). In addition, relative to within a sufficient margin of safety [17]. It is in the anterior subperiosteal area, human mandibles incorporate relatively corpus where humans display the greatest hypertrophy of more bone into the symphyseal region of the anterior corpus cortical bone mass (Figure 5), and since this is where the (Figure 2). difference between ape and human corpus dimensions are The unusually dense packing of bone in the anterior strikingly divergent, this hypertrophy could plausibly be corpus of human jaws does not appear to be explicable as associated with a functional response for reducing masti- an effect of allometric scaling (Figure 3). Whether evaluated catory stresses. This explanation is undermined given that against mandibular length (a general-purpose biomechanical adductor force in humans is probably well below that utilized size proxy owing to its being proportional to bending by Great Apes. That is, humans likely do not produce the moment arms that act during mastication [18–22]) or forces necessary to create mandibular stresses equivalent to total subperiosteal area (Figure 4), recent humans display those in Great Apes given the amount of bone we utilize. more bone than expected given the scaling relationships of Comparative data on muscle force are hard to come by, but hominoids as a whole. Human cortical hypertrophy is thus healthy human subjects may typically produce bite forces in not explicable as the predicted outcome of bone mass in a the range of 350–1235 N [28–32], and theoretical analysis mandible of its particular dimensions. suggests that forces between 700 and 1300 N are possible At least three functional explanations serve as competing [33, 34]. By contrast, gorillas and chimpanzee bite force hypotheses to explain cortical hypertrophy in the modern capability may exceed 1500 N [34], and orangutans are human mandible. These hypotheses are (1) bone mass is probably capable of approaching 2000 N of occlusal force related to shifting masticatory demands in recent human [35]. The higher estimates for humans suggest peak occlusal evolution, (2) bone mass in the mandible is correlated with forces approaching those of chimpanzees but with a more factors influencing cortical bone metabolism systemically, efficient conversion of adductor force into useful bite force. and (3) bone mass is related to the unique human capacity The same craniofacial geometry that leads to this greater for articulate speech. Each of these hypotheses is critically efficiency in humans also reduces the magnitude of bending examined presently. moments acting on the mandible, but whether this implies equivalent or reduced stresses in humans relative to other hominoids depends upon which estimate of bite force is 2.1. Shifting Masticatory Demands. Two important events most reflective of human masticatory behavior. Under an assumption that extraoral food processing is ubiquitous for in human evolution are instrumental to understanding recent changes in masticatory biomechanics. One is that anatomically modern Homo sapiens [26], the theoretically the muscles of mastication became smaller relatively early highest occlusal forces that humans produce are unlikely to be routine. Since adductor forces in humans are reduced in the evolution of Homo, although the cause and timing of this event is disputed [24, 25]. What is likely is that relative to large-bodied hominoids, it is thus reasonable to over the course of human evolution, the ability to produce hypothesize that humans experience relatively low levels of large masticatory forces was compromised. The second event bending stress during mastication [17]. was the advent of extraoral food processing, which today In addition to bending, axial torsion of the corpus is a likely source of stress in human mandibles. The prediction represents a ubiquitous feature of human ecology [26]. A certain effect of this technology, whenever and however it of twisting stress magnitudes, however, is complicated by occurred, is that the production of large occlusal forces the fact that it is difficult to estimate the moment arms in twisting from simple consideration of skull morphology. becomes progressively more unnecessary and less selectively important. Whatever the chain of causality between reduced In absolute terms, torsionalstrengthinhumansisreduced musculature and food processing technology may have relative to Great Apes (Table 1), but when scaled to proxies of available adductor force, Homo wouldappeartoexperience been, the biomechanical effects are straightforward: the genus Homo evolved a masticatory apparatus less capable less stress compared to chimpanzees. Given an assumption of producing largeocclusalforceswithnoapparentcostto that twisting moments in humans are no larger than those in fitness. Great Apes, then it is reasonable to conclude that twisting If one makes the reasonable assumption that the effect, stresses are equivalent, if not lower, in humans relative to apes. if not the intent, of extraoral food processing was to make the bolus less resistant to breakdown (see [27]for While confirmatory data are currently lacking, the pre- explanation of the material parameters involved), then ceding discussion supports the inference that the bending and twisting moments produced by humans do not produce the recent human masticatory environment is relatively benign in terms of the muscular and biting forces that the types of stresses that would account for the amount of Journal of Anthropology 3 0.2 p p g g g 0.15 300 p g g g p p t g p g g g t t t t p p t p 200 t p t g p t 0.1 t hhh h h hh h hh hhhhh hh h Pan Pongo Gorilla Homo 40 60 80 100 120 140 160 180 Figure 1: The ratio of mandibular bone area (mm raised to the 0.5 Mandibular length power) in midsagittal section to mandibular length (mm, measured from infradentale to the intersection of the midsagittal plane with Figure 3: Regression of cortical area in midsagittal section on the gonion-gonion chord)) in samples of adult great apes and mandibular length (r = 0.93) for an adult sample of 100 hominoid humans (N = 10 males and females for each taxon). 25th and mandibles (N = 10 males and females of Pan troglodytes [t],Pongo 75th percentiles (box), median (line), 10th and 90th percentiles pygmaeus [p], Gorilla gorilla [g],Homo [open circles], Hylobates (whiskers) and outliers are shown. For this index, ANOVA is lar and agilis [h]) [23]. The modern human sample (open circles) significant (P < 0.001), and unplanned comparisons show no is superimposed on the hominoid regression. Human mandibles difference among the apes while humans differ from each ape possess more bone than expected based on scaling relationships species at P < 0.05. This finding of significantly greater amount among all hominoids, based on a G-test for the random distribution of bone given jaw length in humans applies throughout the corpus of residuals above and below the regression line (P < 0.001). [17]. 0.8 p g g g 0.6 p 300 p g p g pg g p p g t g p g g t t t t p p t p t p 200 t 0.4 t p hhhhhhh hhh hhhhhhhh 0.2 h 0 200 400 600 800 1000 1200 1400 1600 Pan Pongo Gorilla Homo Subperiosteal area Figure 2: Mandibular bone area (mm ) in midsagittal section as a Figure 4: Regression of cortical area in midsagittal section on fraction of total subperiosteal area in samples of adult great apes subperisoteal area (r = 0.95) for a sample of 100 hominoid and humans (N = 10 males and females for each taxon). 25th mandibles (N = 10 males and females of Pan troglodytes [t],Pongo and 75th percentiles (box), median (line), 10th and 90th percentiles pygmaeus [p], Gorilla gorilla [g],Homo [open circles], Hylobates (whiskers) and outliers are shown. For this index, ANOVA is lar and agilis [h]) [23]. The modern human sample (open circles) significant (P < 0.001), and unplanned comparisons show no is superimposed on the hominoid regression. Human mandibles difference among the apes while humans differ from each ape possess more bone than expected based on scaling relationships species at P < 0.05. This finding of significantly greater bone among all hominoids, based on a G-test for the random distribution packing in humans is most pronounced in the anterior corpus [17]. of residuals above and below the regression line (P < 0.001). bone found in human jaws. Since humans may not expe- The premise of a functional linkage between mandibular rience stress magnitudes equivalent to other anthropoids, bone mass and geometry on the one hand, and masticatory then the hypothesis that cortical hypertrophy in human forces on the other, is merely a specific invocation of the mandibles represents a structural response to masticatory general principle that the developmental loading environ- forces is not compelling. This argument assumes that human ment governs bone modeling [36, 37]. Alterations to bone bone is responsive to mechanical stress in the same manner mass and geometry are the outcome of modeling activity as bone tissue in nonhuman primates. (particularly during growth), while bone remodeling is the 0.5 Cortical area /mandibular length Cortical area/subperiosteal area Cortical area Cortical area 4 Journal of Anthropology stress or strain interval that is “ideal” in that it is the target of metabolic activity. On the other hand, if high- frequency loads, irrespective of magnitude, are associated with increased modeling or remodeling activity, then the metabolic response is less clearly directed to a particular range of stress or strain. There is, however, an abundance of evidence that alteration of load history in terms of frequency, magnitude, or both can engender significant changes in bone mass and/or geometry [41, 45, 46]. It is in this light that comparative differences in bone size and shape are interpreted in a biomechanical framework. In the present context, changes in bone mass (cortical packing) or geometry (the contours of the chin) which have culminated in Figure 5: Cortical bone contours in midline sections of gorilla modern human mandibular morphology are conceptualized (left) and human (right) mandibles. Labial aspect is to the right. as the result of evolutionary changes in patterns of stress. Scale bar is 10 mm. In humans, on average, cortical bone accounts Comparative investigations have assumed that changes in for 49% of the overall area enclosed by the periosteal (outer) relative stress magnitude, rather than frequency, are more boundary of the midline section; in gorillas the average fraction of the total area taken up by cortical bone is about 30%. Because important for explaining the form of the human mandible the overall size of the symphysis is significantly smaller than those [11, 14, 47]. of great apes, the added bone in the human symphysis does not match the absolute strength in great ape mandibles. Scaled to mandibular length (an appropriate biomechanical size proxy), 2.2. Systemic Cortical Robusticity. That bone mass is sensitive humans have on average, relatively stronger symphyses [17]. This to systemic effects of hormonal factors and disease is well does not account for the reduced adductor and biting forces that established. More provocative in the context of human humans produce. Accounting for these factors and the fact that our evolution is that the activity levels that influence certain masticatory demands are reduced due to our practice of extroral regions of the skeleton may produce systemic effects which food processing, human jaws appear to be much stronger than mimic functional adaptation to stress on a local scale. The necessary given the mass and distribution of cortical bone. most explicit articulation of this hypothesis proposes that cranial bone thickness may represent an effect of generalized locomotor or other activity rather than being specifically responsive to one or more cranial functions [48]. In its most Table 1: Torsional strength of hominoid mandibles. distilled form, the hypothesis posits that bone adaptation Taxon Mean Standard error Range T/K ratio to local stress spills over beyond an affected region and produces similar effects throughout the skeleton. Beyond Homo 542 37 292–1072 1.6 Lieberman’s limited experimental data, there is scarce empir- Pan 556 40 314–896 2.4 ical support for this idea, although the absence of support is Pongo 879 68 490–1456 1.1 in some part due to a paucity of experimental designs that Gorilla 1729 102 1198–2808 0.9 specifically evaluate the hypothesis. N = 20 (10 males, 10 females) for each taxon. Means, standard errors and Both Asian Homo erectus and Homo neanderthalensis ranges are for a thin-tube model for torsional strength (K,unitsinmm ), are distinguished from Homo sapiens in terms of skeletal which determines strength as a function of area and minimum wall thickness [17, 44]. Nonparametric ANOVA for mean values of K is significant at robusticity, especially in the cranium, and indeed recent P < 0.001. Post hoc tests reveal that all pairwise comparisons are significant human evolution is associated with skeletal gracilization in with the exception of Homo versus Pan (P > 0.05). The T/K ratio estimates the context of shift in foraging strategy [49]. Diminution torsional shear stress, where T is the applied twisting moment. Since the of the mandible is but one feature of this trend [50, 51]. twisting moment arm is difficult to estimate from skeletal material, the Robusticity can be defined in various ways beyond size, moment arm is assumed constant (1.0, arbitrary units), and the applied force is considered to be the summed estimated forces of the jaw adductors however, including the absolute and relative thickness of the from reference [34]. bones under consideration. In the modern human mandible, the cortical bone is unusually thick by hominoid standards even though corpus size itself is considerably reduced more dominant metabolic activity in adulthood [38]. It is (Figure 5). By this criterion of thick cortices, the modern well established that dynamic rather than static loading is human mandible is “robust” in the same way as, for example, implicated in bone metabolic activity [39]. Some models of Neanderthal long bones. Yet this phenomenon of thick bone modeling emphasize strain magnitude as important mandibular bone is not part of a general skeletal feature [40, 41], while experimental data is accumulating that in modern humans because the remainder of the cranio- implicates strain frequency as an important stimulus for facial skeleton is not characterized by cortical hypertrophy. bone formation [42, 43]. The interaction of these variables Consequently, whatever factors underlie systemic skeletal is also an important consideration. robusticity, the human mandible cannot be explained by If strain magnitude represents the stimulus for bone their effects as the packing of bone in the jaw is atypical of formation or resorption, then conceptually there exists some the remainder of the skeleton. Journal of Anthropology 5 2.3. Bone Mass in the Mandible Relates to Speech. The idea observed [64]. Assuming that the transition between syllables that relatively thick cortical bone in the human mandible involves mandibular movements and altered recruitment could be functionally related to speech is nonintuitive in that of the masticatory, suprahyoid, and Genioglossus muscles, phoneme articulation is a low-stress activity compared to these observed rates may provide a first approximation of the mastication. That is, if mastication of unprepared, uncooked loading frequency of the mandible during spoken language. food among apes does not produce cortical hypertrophy Given this assumption, the loading frequency during speech in their mandibles, why should we expect speaking to be may be from 3–5 times greater than those of mastication. causal in producing thick bone in ours? In fact, activities Mandibular bone strain in mastication or speech is not such as talking have been suggested to be a critical consid- known from human subjects. Theoretical modeling studies eration for understanding the relationship of the functional suggest that the difference in strain magnitude between linkage of physiological activity and bone morphology [52]. mastication and speech may exceed two orders of magnitude Accumulating evidence suggests that high-frequency, low- [65, 66]. The anatomical relationships of the masticatory and amplitude strains strongly influence bone metabolic activity suprahyoid musculature to the maxilla and mandible suggest [42, 52, 53], such that introduction of novel loading regimes that the low-amplitude, high-frequency loads associated with involving low magnitude strains (5 με or below) at high speechwillprimarily affect mandibular rather than maxillary frequencies (∼30 Hz) is sufficient to produce significant bone. There are two reasons to suspect that this is true. First, increases in trabecular density and number, bone volume of the extrinsic tongue muscles, Genioglossus originates on fraction, and bone formation rate. These data suggest strain the mandible, and the others have no direct attachment to frequency has an important role in the determination of the maxilla (Hyoglossus, Styloglossus, and Palatoglossus). bone structure. While most work in this area suggests that Second, the opening and closing movements of the mandible cancellous bone formation is most dramatically affected by involve subtle but measurable changes in the width of the imposition of low-magnitude, high-frequency loads, this mandibular arcade owing to the masticatory muscles acting type of loading regime has produced increases in cortical upon it to the exclusion of the maxilla. The lines of action bone mass in human subjects [54]. of the Masseter and Temporalis include a lateral component, The critical question is whether speech produces the and those of the lateral and medial pterygoids include a kind of loading environment that is conducive to sustained medial component (though their primary actions differ, in bone formation in the human mandible, and if talking is that only Lateral Pterygoid is involved in jaw opening [67]). to be uniquely implicated in bone hypertrophy, the loads These small components produce transverse bending during produced must be distinct from those encountered in mas- jaw opening and closing in nonhuman primates [68]. ticatory activity. Human language does involve utilization If the hypothesis that bone hypertrophy in the human of the muscles of mastication to produce the mandibular mandible is functionally related to speech is true, then it movements involved in speech production [55], but at must explain why this hypertrophy is most pronounced in daily cycle numbers which may routinely exceed those the anterior corpus, whereas the distribution of bone is less associated with feeding. The complex movements of the distinct from other hominoids in the postcanine corpus. tongue required for phoneme production likely involve There are two effects of language use, one local and one continuous activity in suprahyoid muscles with mandibular remote, which can be postulated to explain this. First, both insertions, most notably Genioglossus [56, 57]. Because the Genioglossus and the anterior belly of the Digastric insert mandible is moved without resistance during speaking and on the lingual inferior symphysis: the former muscle is more the glossal musculature is relatively diminutive with respect or less constantly active in speech, and the latter is used for to the mass of the mandible, speech would appear to be positioning the jaw during certain speech tasks [69]. The capable of imposing low-magnitude stresses at relatively high forces exerted by these muscles on the symphyseal bone are frequency. dynamic and low and probably have negligible impact on the Chewing cycle frequency in humans averages about strain field in the postcanine region. Second, the actions of 1.4 Hz [58], with a range of 1.2–1.7 for masticating foods the masticatory muscles in positioning the mandible during of various hardness [59]. Speech rates will obviously be speech tasks will produce small transverse bending moments variable, and one concern is what should count as a speech that will have their largest effects in the anterior rather than “cycle” in the intended biomechanical context. In a study the posterior corpus. contrasting masticatory movements with an artificial speech The preceding points should not be taken to mean task, duration of opening and closing movements was that the biomechanical impact of speech is confined to the significantly lessened in speech [60], supporting the idea anterior corpus. Other muscles important in speech produc- that speech “frequency” is typically greater than masticatory tion (e.g., Mylohyoid) probably have local effects at their frequency. Speech rates have been quantified to 3.5–6.5 insertions, although the overall geometry of the mandible syllables/s [61]) and 6.7 morae/s [62]. From polysyllabic makes it unlikely that anything other than the muscles of English word durations of native and nonnative speakers, mastication produce significant bending or twisting of the rates between 4.5–5.0 syllables/s are observed [63]. Inves- jaw during speech. Any such moments induced in speech tigation of speaking rate over 5,000 utterances (over four will have global effects in the sense that they influence hours of data) suggest similar rates but underscore the the strain field all along the corpus, but these effects will variability intrinsic to conversational speech in that a range not be uniform. One of the most striking features of the of values from over 1 to nearly 10 syllables/second can be human mandible is that given overall size, there is more 6 Journal of Anthropology bone than expected everywhere in the corpus [17]. This is of its size relative to moment arm and force proxies. Because consistent with the observation that the masticatory muscles this type of comparison is necessarily intraspecific, the are intimately involved with speech, because their actions analysis represents an extreme case of narrow allometry, will have stress effects throughout the mandible. Based and high correlations are not expected even if a significant on anatomical relationships and biomechanical principles, bivariate relationship is observed. Figures 6, 7,and 8 relate strains arising from speech activity will likely be highest in chin size to those variables which are expected to covary with the region of the chin—that uniquely human trait which it if mitigation of masticatory stress is important in modern allows us to identify ourselves in the fossil record. This humans. In each case, this covariation is sufficiently tenuous observation then prompts the question of whether the chin that we may reasonably suppose that the relationship is weak itself is related to the acquisition of spoken language. if it exists at all. In the case of significant regression of chin size on bicanine breadth, this does correspond to the idea that coronal bending is the critical load influencing the 3. Revisiting the Chin Problem human anterior corpus [14], but as chin size is explained by a mere 4% of the variance in bicanine breadth, this The idea that the human chin is the product of language apparent relationship may equally plausibly be interpreted as is not new [8, 9], and the hypothesis is still being explored acorrelatedeffect of somatic size [76]. These observations, in today [7]. It is an attractive hypothesis in that it ties together addition to the foregoing point that both force and bending two unique human attributes in a single functional package. moment production are probably highly reduced in recent The evolutionary significance of the chin has been pondered humans, weaken the hypothesis that the human chin is foroveracentury(reviewed in refs.[14, 16]), but the recent primarily a response to altered masticatory biomechanics. literature on the subject is divided among essentially four points of view: (1) the chin represents an adaptation to a novel and unique biomechanical environment [14, 70]; 3.2. The Chin Results from Sexual Selection. The dimorphism (2) the chin is the result of sexual selection [71, 72]; (3) of the human chin continues to fuel speculation that it is the chin is but a structural artifact having no important maintained as an object of sexual selection [71], not an biomechanical function [73]; (4) the chin is a structural unreasonable view considering its sex-specific characteristics response to the physiology of speech [7]. [77]. A critical issue is how variation in the bony form of The cortical hypertrophy of the anterior corpus has no the chin influences its appearance in terms of physiognomy. necessary connection to the presence and form of the chin; That is, the chin may be important in its role in shaping however, it is theoretically possible that the distribution patterns of symmetry in the human face rather than in of bone and the geometry of the region are part of a the details of its configuration [72]. In juxtaposing the single functional complex. It is therefore prudent to evaluate sexual selection hypothesis against the masticatory stress whether by explaining the bone packing that is apparently hypothesis, if the bony conformation of the chin is the result unique to humans, the function (or lack thereof) of the chin of sexual selection to the exclusion of masticatory or other might also be revealed. biomechanical stress, males and females might be expected to display divergent morphologies relative to measures of size and shape. Whether the salience of the bony chin in 3.1. The Chin Results from Masticatory Biomechanical Factors. profile (Figure 9) or its shape and size relative to mandibular I argued previously that the chin was the result of changes size (Figures 10 and 11) is considered, there appears to be in human jaw proportions which lessened the impact of no consistent difference between the sexes in midsagittal wishboning strains but did not mitigate another important section, which is the appropriate perspective in evaluating source of masticatory stress, coronal bending of the anterior biomechanical effects. Similarly, there is no indication that corpus by twisting of the postcanine corpora [14]. The there are significant sex differences in humans with respect validity of this hypothesis had certain predictable outcomes. to bone structural properties [16]. If the chin is the product First, the emergence of the chin in the genus Homo would of sexual selection, it has not resulted in obvious differences be closely tied to changes in jaw size and architecture. in biomechanical performance between males and females, Subsequent investigation has shown that support for this is despite the fact that postadolescent growth of the mandible equivocal [15]. Implicit also is the assumption that having is distinct between males and females [78]. The hypothesis a discernible chin confers a mechanical advantage under of sexual selection, however, does not easily lend itself to the critical load (coronal bending) than a mandible lacking explanations of bone hypertrophy [14]. this feature. The results of recent finite-element modeling studies [74, 75] are in conflict on this point. It is thus unclear whether, once size is controlled, the morphology of 3.3. The Chin Is a Structural Artifact. The chin was featured the chin confers a mechanical advantage over a hypothetical as an example of a nonadaptive character in Gould and “nonchinned” morphology. Certainly, the chin does serve to Lewontin’s [80] critique of adaptationism. In that paper, stiffen the anterior corpus, but whether it must therefore the chin was described as the result of interacting growth represent an adaptation to shifting masticatory demands fields without any necessary functional utility; in essence, remains an open question [74]. a necessary but (in itself) selectively unimportant artifact If the chin is a structural response to masticatory of development. While the possibility cannot be denied, as function, there are predictions that follow in terms of scaling explanation this is unsatisfactory since there is no skeletal Journal of Anthropology 7 300 300 200 200 150 150 20 22 24 26 28 30 32 34 60 65 70 75 80 85 90 95 Jaw length Bicanine breadth Figure 6: Chin size relative to mandibular length for a mix- Figure 8: Chin size (mm ) relative to bicanine breadth (mm) for a sexed sample of adult modern humans from the Tigara (N = mixed-sex sample of adult modern humans from the Tigara (N = 57) andElHesa(N = 51) collections housed at the American 57) and El Hesa (N = 51) collections. Daegling [14] hypothesized Museum of Natural History. Mandibular length (mm) represents a that bicanine breadth would covary positively with chin size as this general biomechanical size proxy, such that if forceful mastication is represented the portion of the anterior corpus loaded in coronal important in determining corpus size, the expectation is for positive bending due to twisting of the postcanine corpora. Regression is correlation between the variables. Regression is nonsignificant (P = significant at P = 0.04; however, r = 0.04, indicating that little 0.12) indicating an absence of such a relationship. Chin size (units of the variation in chin size is explicable by variation in bicanine in mm ) is determined as a simple product of midsagittal height and breadth. chin thickness at the tuber symphyseos; that is, there is no accounting for subperiosteal bone area in these measurements. The Egyptian El Hesa sample dates between 200–400 AD; the Tigara sample derives from Point Hope, Alaska between 1200–1700 AD. M 3.5 3 F M M M F 2.5 M FF M M F F F M F F F F M 300 2 F M M F FF F FF M F F M M M F F M FMM 1.5 M F M F F F M 0.5 M 11 12 13 14 15 16 17 18 19 Chin thickness Figure 9: The depth of the anterior incurvatio of the human chin (units in mm) is contrasted with the thickness of the chin (mm) at the tuber symphyseos in the Tigara sample. Thickness is measured perpendicular to the vertical tangent at the most anterior point 300 400 500 600 700 800 900 of the symphyseal tuber; this measurement will be approximately Temporal fossa size (mm ) parallel to the occlusal plane. Sexing for the sample is based on Costa [79] who employed multiple criteria including features of the Figure 7: Chin size relative to temporal fossa size for a mixed-sex os coxae. A deep incisura generally gives the appearance of a more sample of adult modern humans from the Tigara (N = 57) and salient chin, while chin thickness provides a size measure with no El Hesa (N = 51) collections housed at the American Museum necessary indication of distinctiveness. Interestingly, the different of Natural History. Chin size is determined as a simple product shapes said to differentiate males from females are not reflected of midsagittal height and chin thickness at the tuber symphyseos, by these measures, that is, there is substantial overlap of the sexes. and temporal fossa size is likewise the product of fossa length and Thus, there is no definitive sex difference in shape (as measured breadth. If temporal fossa size is proportional to temporalis cross- here) of the chin in midsagittal section. Nevertheless, regression sectional area, this variable serves as a proxy for adductor force, is significant (P = 0.02), indicating that large chins are also more meaning that positive correlation of chin size and fossa size is salient, in that they are associated with larger anterior incisures. expected if masticatory mechanics are functionally linked to corpus Comparison of sexes by analysis of covariance (ANCOVA) reveals morphology. Regression is nonsignificant (P = 0.50), suggesting a no significant difference between male and female slopes (P = 0.90) lack of functional relationship. or intercepts (P = 0.14). Chin size (mm ) Chin size (mm ) Incisura mandibulae anterior depth Chin size (mm ) 8 Journal of Anthropology 0.52 0.5 M M 200 F F 0.48 F 180 M M M 0.46 F F M M F F F M MF F F 160 M F M 0.44 F F F F M M M M 140 F 0.42 M M F F M F M M F M F M M M M F F F F F F F M M 0.4 M F F F F F 120 F F M F F M F M F M F 0.38 F F F FF 100 F F M 0.36 F F F F 80 0.34 0.32 60 65 70 75 80 85 90 95 65 70 75 80 85 90 95 Jaw length Jaw length Figure 11: Chin size (determined as the product of height and Figure 10: An index of chin breadth/height (“shape”) is contrasted breadth) is positively associated with jaw length (P < 0.001; r = with a measure of jaw size (mandibular length, units in mm) 0.24), with substantial overlap of the sexes in both variables. This for the Tigara sample. Sexing for the sample is based on Costa significant finding is suggestive of a functional relationship, but [79]. Regression is nonsignificant (P = 0.15), indicating that the the correlation is plausibly reflected as a general effect of body general geometry of the human symphysis is insensitive to size. The size dimorphism. Daegling’s [14] model of the masticatory loading female sample range encompasses the male range for shape. Thus, of the chin emphasized coronal bending of the anterior corpus shape differences are not apparent between the sexes in midsagittal due to twisting of the postcanine corpora. Torsion of the corpora, section. Comparison of sexes by analysis of covariance (ANCOVA) however, has no necessary scaling relationship with mandibular reveals no significant difference between male and female slopes length. Alternatively, this relationship could reflect a structural (P = 0.89) or intercepts (P = 0.68). response to wishboning strains [68], although it is not known whether this load occurs in human mastication. Comparison of sexes by analysis of covariance (ANCOVA) reveals no significant feature that cannot be assessed in exactly the same terms; that difference between male and female slopes (P = 0.47) or intercepts is, every morphological feature can be accurately described (P = 0.21). as developmentally determined. The finding of cortical hypertrophy does refocus the issue somewhat: why would a mere artifact be associated with such a heavy metabolic reduction. To some degree, the apparently exceptional investment (assuming the form of the chin and the bone enamel thickness in modern humans can be explained in this beneath it have something to do with one another)? way [82, 83]. If this is the correct interpretation, however, With certain specific considerations, the idea of the form a mechanobiological role for modulation of bone mass is of the chin having nothing much to do with mechanical denied or at least requires an exception in the modern human function is more plausible. Weidenreich [13]offered a com- case. This amounts to special pleading in the absence of pelling, but very simple, explanation for the chin’s salience. specific tests. He noted that modern human incisors are highly reduced relative to earlier hominins or for that matter, hominoids. The human chin is thus the consequence of reduced alveolar 3.4. The Chin and Language. The latest contribution to the support for diminutive teeth. The appearance of the chin, role of language in determining the form of the chin is the therefore, will coincide with incisor root reduction in human finite-element study of Ichim et al. [7]. Noting that their evolution. This explanation by itself fails to explain why previous iterations [75] showed no advantage to the chin for the basal portion of the symphysis protrudes anteriorly; masticatory stress, they argued that in a hypothetical non- that is, its persistence conceivably betrays some functional chinned mandible, the action of Genioglossus muscle at a imperative. Krantz [81] opined that space was at a premium particular orientation produced elevated stresses along the in the modern human oral cavity, essentially arguing that the labial anterior corpus reminiscent of the trigonum mentale basal portion of the mandible could not retract and still leave that typifies many human chins. From this, they suggested sufficient room for the oral viscera. Weidenreich’s position that the appearance of language precipitated the formation is particularly germane to the question of the form of the of the chin. chin and inferences about function, because it underscores As noted above, the small strain magnitudes that are the possibility that the chin itself is the result of separate produced in speech may not disqualify the idea that this functional requirements. activity could influence the distribution of bone tissue. Similarly, there is the possibility that cortical hypertrophy Instead, the real issue with this study is whether the isolated in recent humans is an allometric artifact that requires no action of Genioglossus (and its inferred line of action) biomechanical or adaptive explanation. It simply may be provides a realistic load case for spoken language. As several that bone volume in human mandibles is phylogenetically other muscles are involved, this would seem to be unlikely. conserved, while the overall size of the corpus has undergone More importantly, it is also doubtful that Genioglossus is the Chin “shape” Chin size Journal of Anthropology 9 sole culprit for the chin in light of other data concerning structural (and perhaps functional) complex, depending on the muscle’s function. Acting to protrude the tongue, the one’s definition of the chin. Fukase’s [70]work, however, genioglossus is critical for prevention of tongue relapse which indicates that cortical packing characterizes the basal sym- could obstruct the airway of the oropharynx. Consequently, physis as a whole, and the lingual basal region (i.e., in the the muscle is active during respiration and particularly vicinity of the genial spines) is where cortical bone is thickest. during inspiration in alert humans [84]. During sleep, the Thick cortical bone is not a requirement for the mentum muscle shows more or less continuous activity, elevated dur- osseum. ing inspiration, with the exception of intermittent quiescent activity during REM sleep [85, 86]. Consequently, activity 4. Testing the Speech Hypothesis in the Genioglossus is producing low-level strains in the mandible whether or not speaking is taking place. Despite the One apparent problem with the speech hypothesis is that the uniqueness of their laryngeal space, humans do not appear to load frequencies inferred above for speech are still very low be idiosyncratic in recruiting Genioglossus for maintaining compared to the experimental conditions under which bone respiratory airflow [87, 88]. Frequent and ubiquitous activity tissue responds to low-strain magnitudes (30 Hz). If speech in Genioglossus is thus not particular to humans, even produces load frequencies of over 5 Hz, this is close to the if the activity of this muscle during speech is; therefore, lower bound of bone sensitivity to low-magnitude strains the mechanobiological stimulus of this muscle with respect [42] but well below the ideal frequencies for inducing bone to mandibular bone is probably not sufficiently unique augmentation [92]. There are, however, two considerations in people to suppose that it alone counts for symphyseal that suggest that the physiology of speech could effectively morphology. induce bone formation. First, it may be the result of actions There are additional interpretive problems with Ichim associated with the muscles involved in speech but not et al.’s [7] model. By ignoring the suprahyoid muscles as necessarily those confined to the active production of speech. well as those from the trigeminal and facial somitomeres, Muscle activity occurring during relatively nonvigorous but the loadcase that induces the stress field that they accord ubiquitous events (e.g., in maintaining mandibular “pos- significant is highly unrealistic and unsupported by inde- ture”) is implicated in producing high-frequency (10–50 Hz) pendent data. Recruitment of these other muscles which are but low-amplitude strains that appear to be important in known to function during speech [55, 56, 89] necessarily stimulating bone formation [52, 93]. Since the structural changes the details of the stress field in the anterior corpus. characteristics of human muscles involved in speech differ Determining the accuracy of a modeled stress field is a from their homologues in nonhuman primates [94], then formidable task, but even with such a depiction, relating the effects of these muscles in postural maintenance may the details of stress magnitudes and gradients to the specific be qualitatively distinct. A second consideration is that the details of chin morphology is even more challenging. bone literature is replete with examples of dynamic loads Furthermore, anecdotal observation suggests that the mere of varying magnitudes and frequencies having measurable appearance of the chin has no necessary connection to effects on bone modeling and remodeling. Clearly, the language use, regardless of underlying bony morphology. skeleton can respond to a range of combinations of load Angelman’s syndrome is a developmental disorder in which frequency and magnitude [45]. If bone is sensitive to the severe limitation or absence of spoken language is one interplay of daily loading cycles and average cyclical peak symptom, yet individuals presenting with this syndrome are strains, speech may provide a potent stimulus for bone described as having prominent chins [90]. formation that is unusual among primates. It has been Finally, it should be recognized that the semantics of emphasized that the ability of low strains to engender the “chin problem” do matter for its resolution [16]. If one metabolic response in bone is intimately tied to the number defines the chin by criteria of the tuber symphyseos, tubercula of loading cycles per day [52, 92]. Given the discussion of lateralia, and the incurvatio mandibularis, identifying a frequencies above, the number of loading cycles per day biomechanical milieu which accounts for this constellation owing to speech may be orders of magnitude higher than of features is exceedingly difficult. On the other hand, if one those associated with mastication. While the appropriate accepts the heuristic definition that it is “but a blob of bone” data are lacking, a thought experiment may underscore [11, page 4] then deciding its evolutionary significance is a the plausibility of the speech hypothesis. Assuming a load tidier endeavor, if not more imprecise. Focusing exclusively frequency of 5 Hz, speaking for 5–10 minutes an hour for on the property of bone mass, the mystery of the chin still 16 hours produces 24,000–48,000 loading cycles in a single prevails; it is likely that there is more bone here than we need. day. This range encompasses the 36,000 cycle daily stimulus Our confusion stems from the underlying assumption that that can promote bone activity with strains as small as 5– the goal of bone formation and maintenance is to make sure 10 με [52, 95]. Unresisted opening of the jaws in macaques that bones are exactly as strong as they need to be. Natural creates bending strains of ∼100 με, and licking behaviors selection need not lead to this state of affairs [91]. create strains between 100–300 με [68]. Even granting the What is important to disentangle is whether cortical excessive amount of bone in human jaws, it appears likely hypertrophy itself explains the human chin. If bone hyper- that strains engendered during speech would exceed 5 με. trophy is localized at the labial swelling of the human A desired initial test of the speech hypothesis is the exam- symphysis (tuber symphyseos), then the chin and cortical ination of the assumptions recruited in the above argument. hypertrophy could be reasonably viewed as part of a single That is, how do speech rates and frequencies compare with 10 Journal of Anthropology those of mastication over day-to-day intervals? Modeling the bution in the anterior corpus is relatively meager. Specimens which preserve the symphyseal region (e.g., the SKW 5 actions and activity of all the muscles involved with speech mandible of Paranthropus robustus) may nevertheless not is obviously an involved undertaking, but without such preserve the internal contours of bone very well due to information the nature of loads and the concomitant stresses factors of fossilization [99]. The anterior corpus of SK 15 in the human mandible, the biomechanical effects of speech (the type of “Telanthropus,” likely an early species of Homo)is will remain uncertain. In general terms, the details of bone unlike that of modern humans in terms of geometry (i.e., it deployment in the human mandibular corpus would suggest lacks a discernible chin) but occupies the lower end of the thatspeechproducesstresspatternswhich inducemodeling modern human range in terms of cortical area, relative to and remodeling that are for the most part localized in the both subperiosteal area and mandibular length [23]. Homo anterior corpus. Theoretical or experimental evidence to the floresiensis mandibles are quite unlike modern humans in contrary would undermine the hypothesized relationship. terms of symphyseal morphology and relative corpus size; A second test is developmental: assuming the pattern published CT images do not indicate the modern human of cortical bone distribution is not established in utero or pattern of cortical hypertrophy, at least in the postcanine prior to language acquisition, the adoption of speech may corpus [100]. Neanderthal mandibular remains have been be associated with ontogenetic changes in bone mass in the examined by computed tomography [101, 102], so at least corpus. The weakness of this test, however, is in these initial some data needed to investigate cortical packing in H. assumptions that the general pattern of bone distribution is neanderthalensis are already collected. A finding of cortical developmentally labile in the extreme. There exist data to hypertrophy in mandibles lacking a chin among Pleistocene suggest that this is a na¨ıve premise and that skeletal mass and Homo in association with indications of symbolic behavior geometry are subject to species-specific canalization [96], (e.g., [103]) would suggest that the modern human chin is despite the capacity for bone to change mass and geometry not a diagnostic feature of articulate speech. developmentally. Bone packing in the human symphysis, despite being quantitatively distinct from other primates, is 5. Rethinking Functional Adaptation still highly variable in that the fraction of symphyseal cross- sectional area occupied by cortical bone can range from 32– The distilled version of Wolff ’s Law, that maximation of 72% [17]. Given the difficulties facing us in interpreting strength with a minimum of material is the selective target the relationship of skeletal form to physiological activity of bone metabolic activity, has been rightly criticized in [97], we should be loath to assume that most of this recent years owing to an accumulation of contrary data variance in relative bone thickness is explained primarily [44, 97, 104–106]. The idea that bone morphology represents by whether an individual was verbose or taciturn. Given a structural solution to minimize biomechanical stress is no experimental designs that have uncovered the influence of longer tenable, but what exactly is being optimized in the high-frequency strains to bone metabolism, one hypothesis skeleton is enigmatic [93]. Whether the proposed linkage worth exploring is that the onset of speech activity is of speech to mandibular bone distribution is valid or not, associated with increases in mandibular bone mass. Certainly what seems clear is that bone deployment in the mandible is suckling activity immediately provides a high-frequency, suboptimal with respect to a criterion of obtaining a globally low-magnitude environment in all mammals postnatally, but constant relationship between stress and strength. Perhaps the developmental timing in human speech acquisition is what we are observing is instead a general strategy of bone sufficiently narrow that our discrimination of a temporally adaptation in which the particulars of a loadcase are less specific period of bone hypertrophy should be possible. important that the general dynamic features of a loading regime, such that the metabolic activity of bone is effective The implications of this hypothesis—that articulate but not necessarily economical with respect to structural speech underlies cortical hypertrophy in human mandi- integrity. bles—for paleoanthropological inference are large, but the current absence of supportive data means that its application to the fossil record is largely speculative. There is, however, 6. Conclusions one scenario which itself could provide an important, if not decisive, test. Given that language is a symbolic capacity and High-frequency, low-magnitude loads associated with artic- that some aspects of material culture have unmistakable sym- ulate speech are hypothesized to explain the apparent bolic content, it is reasonable to assume that the presence of paradox of hypertrophied mandibular bone in contrast to symbolic, nonutilitarian artifacts is indicative of the capacity the reduced bone thickness that typifies the remainder for language. The presence of a nonhuman pattern of bone of the modern human skull. Current understanding of distribution in hominin mandibles which are associated bone metabolic activity is consistent with the hypothesis with symbolic artifacts would essentially refute the speech that speech production accounts for the relatively greater hypothesis. Alternatively, provided supportive experimental bone volume that typifies human mandibles in contrast to and developmental data are collected, the observation of nonhuman primates. The detection of elevated bone mass in cortical hypertrophy in the human fossil record could fossil mandibles may thus provide insight into the origins of productively inform questions of the appearance of modern speech in human evolution. human behaviors [98] through inference of language ability. The fact that the greatest concentration of cortical bone Despite the abundance of mandibular remains in the within sections is most apparent in the anterior mandible hominin fossil record, information on cortical bone distri- is consistent with inference of the general effects of jaw Journal of Anthropology 11 loading during speech. Bending moments from the muscles [10] R.H. Biggerstaff, “The biology of the human chin,” in OrofacialGrowthand Development,A.ADahlberg andT.M. of mastication will be largest in midsagittal section and Graber, Eds., pp. 71–87, Mouton, Paris, France, 1977. Geniohyoid, Genioglossus and Anterior Digastric muscles, [11] E.L. DuBrul and H. Sicher, The Adaptive Chin,Charles C. which are intimately involved in speech production, directly Thomas, Springfield, Ill, USA, 1954. attach in this region as well. [12] T. T. Waterman, “The evolution of the chin,” American This hypothesis is testable by different means, but at Naturalist, vol. 50, pp. 237–242, 1916. present it is not directly supported by experimental, devel- [13] F. Weidenreich, “The mandibles of Sinanthropus pekinensis: opmental or comparative data. Instead, the observations a comparative study,” Palaeontologica Sinica Series D, vol. 7, on bone mass in human mandibles are merely consistent pp. 1–164, 1936. with the idea that the mechanobiology of speech can effect [14] D. J. Daegling, “Functional morphology of the human chin,” bone formation to a significant degree. In addition, whether Evolutionary Anthropology Issues, News, and Reviews, vol. 1, bone hypertrophy is functionally linked to the evolutionary no. 5, pp. 170–177, 1993. appearance of the chin remains an open, and to some degree [15] S. D. Dobson and E. Trinkaus, “Cross-sectional geometry and separate, question. morphology of the mandibular symphysis in Middle and Late Pleistocene Homo,” Journal of Human Evolution, vol. 43, no. 1, pp. 67–87, 2002. Acknowledgments [16] J. H. Schwartz and I. Tattersall, “The human chin revisited: what is it and who has it?” Journal of Human Evolution, vol. Data collected for this project was supported in part by 38, no. 3, pp. 367–409, 2000. NSF (BNS 8920592 and BCS 0922429) and by an American [17] D. J. Daegling, “Relationship of bone utilization and biome- Museum of Natural History Collection Study grant to the chanical competence in hominoid mandibles,” Archives of author in 1992. The author also wishes to thank Ian Tattersall Oral Biology, vol. 52, no. 1, pp. 51–63, 2007. and Gary Sawyer for their support and assistance during my [18] W. L. Hylander, “Mandibular function and biomechanical stay at the museum. K. Kupczik and an anonymous reviewer stress and scaling,” Integrative and Comparative Biology, vol. provided helpful critique and commentary on a previous 25, no. 2, pp. 315–330, 1985. draft. [19] M. J. Ravosa, “Jaw morphology and function in living andfossilOld Worldmonkeys,” International Journal of Primatology, vol. 17, no. 6, pp. 909–932, 1996. References [20] M. J. Ravosa, “Size and scaling in the mandible of living and [1] W. L. Jungers, A. A. Pokempner, R. F. Kay, and M. Cartmill, extinct apes,” Folia Primatologica, vol. 71, no. 5, pp. 305–322, “Hypoglossal Canal Size in Living Hominoids and the Evolution of Human Speech,” Human Biology, vol. 75, no. 4, [21] M. Bouvier, “Biomechanical scaling of mandibular dimen- pp. 473–484, 2003. sions in New World Monkeys,” International Journal of [2] B.Arensburg,L.A.Schepartz,A.M.Tillier,B.Vandermeer- Primatology, vol. 7, no. 6, pp. 551–567, 1986. sch, and Y. Rak, “A reappraisal of the anatomical basis for [22] M. J. Ravosa, “Structural allometry of the prosimian speech in middle Palaeolithic hominids,” American Journal of mandibular corpus and symphysis,” Journal of Human Evo- Physical Anthropology, vol. 83, no. 2, pp. 137–146, 1990. lution, vol. 20, no. 1, pp. 3–20, 1991. [3] D.Degusta,W.H.Gilbert,and S. P. Turner,“Hypoglossal [23] D.J. Daegling, Geometry and biomechanics of hominoid canal size and hominid speech,” Proceedings of the National mandibles, Ph.D. dissertation, State University of New York, Academy of Sciences of the United States of America, vol. 96, Stony Brook, NY, USA, 1990. no. 4, pp. 1800–1804, 1999. [24] M. A. McCollum,C.C.Sherwood,C.J.Vinyard,C.O.Love- [4] R.F.Kay,M.Cartmill, andM.Balow,“Thehypoglossalcanal joy, and F. Schachat, “Of muscle-bound crania and human and the origin of human vocal behavior,” Proceedings of the brain evolution: the story behind the MYH16 headlines,” National Academy of Sciences of the United States of America, Journal of Human Evolution, vol. 50, no. 2, pp. 232–236, 2006. vol. 95, no. 9, pp. 5417–5419, 1998. [25] H. H. Stedman, B. W. Kozyak, A. Nelson et al., “Myosin gene [5] J. T. Laitman and R. C. Heimbuch, “The basicranium of Plio- mutation correlates with anatomical changes in the human Pleistocene hominids as an indicator of their upper respira- lineage,” Nature, vol. 428, no. 6981, pp. 415–418, 2004. tory systems,” American Journal of Physical Anthropology, vol. [26] R. Wrangham and N. Conklin-Brittain, “Cooking as a 59, no. 3, pp. 323–343, 1982. biological trait,” Comparative Biochemistry and Physiology A, [6] P. Lieberman, J. T. Laitman, J. S. Reidenberg, K. Landahl, and vol. 136, no. 1, pp. 35–46, 2003. P. J. Gannon, “Folk psychology and talking hyoids,” Nature, [27] K. R. Agrawal, P. W. Lucas, J. F. Prinz, and I. C. Bruce, vol. 342, no. 6249, pp. 486–487, 1989. “Mechanical properties of foods responsible for resisting [7] I. Ichim, J. Kieser, and M. Swain, “Tongue contractions food breakdown in the human mouth,” Archives of Oral during speech may have led to the development of the Biology, vol. 42, no. 1, pp. 1–9, 1997. bony geometry of the chin following the evolution of [28] L. M. Waugh, “Influence of diet on the jaw and face human language: a mechanobiological hypothesis for the of the American Eskimo,” Journal of the American Dental development of the human chin,” Medical Hypotheses, vol. 69, Association, vol. 24, pp. 1640–1647, 1937. no. 1, pp. 20–24, 2007. [29] E. Helkimo, G. E. Carlsson, and M. Helkimo, “Bite force and [8] A. Keith, Antiquity of Man, Williams and Norgate, London, state of dentition,” Acta Odontologica Scandinavica, vol. 35, UK, 1916. no. 6, pp. 297–303, 1977. [9] O. Walkhoff, “Die menschliche Sprache in ihrer Bedeutung [30] G. J. Pruim,H.J.deJongh,and J. J. TenBosch,“Forces acting fur die funktionelle Gestalt des Unterkiefers,” Anatomischer on the mandible during bilateral static bite at different bite Anzeiger, vol. 24, p. 129, 1904. 12 Journal of Anthropology force levels,” Journal of Biomechanics, vol. 13, no. 9, pp. 755– [48] D. E. Lieberman, “How and why humans grow thin skulls: 763, 1980. experimental evidence for systemic cortical robusticity,” American Journal of Physical Anthropology, vol. 101, no. 2, pp. [31] D. P. Sinn, E. A. de Assis, and G. S. Throckmorton, “Mandibular excursions and maximum bite forces in patients 217–236, 1996. with temporomandibular joint disorders,” Journal of Oral [49] C. S. Larsen, Bioarchaeology: Interpreting Behavior from the and Maxillofacial Surgery, vol. 54, no. 6, pp. 671–679, 1996. Human Skeleton, Cambridge University Press, Cambridge, [32] M. C. Raadsheer, T. M. G. J. van Eijden, F. C. van Ginkel, UK, 1997. and B. Prahl-Andersen, “Contribution of jaw muscle size and [50] D. C. M. Boyd, A Functional Model for Masticatory-Related craniofacial morphology to human bite force magnitude,” Mandibular, Dental, and Craniofacial Microevolutionary Journal of Dental Research, vol. 78, no. 1, pp. 31–42, 1999. Change Derived from a Selected Southeastern Indian Skeletal Temporal Series, University of Tennessee, Knoxville, Tenn, [33] B. Demes and N. Creel, “Bite force, diet, and cranial morphology of fossil hominids,” Journal of Human Evolution, USA, 1988. vol. 17, no. 7, pp. 657–670, 1988. [51] C. S. Larsen, “The anthropology of St. Catherine’s Islandpp. [34] S. Wroe,T.L.Ferrara,C.R.McHenry,D.Curnoe, and 3. prehistoric human biological adaptation,” Anthropological Papers of the American Museum of Natural History, vol. 57, U. Chamoli, “The craniomandibular mechanics of being human,” Proceedings of the Royal Society B, vol. 277, no. 1700, no. 3, pp. 155–276, 1982. pp. 3579–3586, 2010. [52] C. Rubin, A. S. Turner, C. Mallinckrodt, C. Jerome, K. Mcleod, and S. Bain, “Mechanical strain, induced noninva- [35] P. W. Lucas, C. R. Peters, and S. R. Arrandale, “Seed-breaking forces exerted by orang-utans with their teeth in captivity and sively in the high-frequency domain, is anabolic to cancellous bone, but not cortical bone,” Bone, vol. 30, no. 3, pp. 445–452, a new technique for estimating forces produced in the wild,” American JournalofPhysicalAnthropology,vol. 94, no.3,pp. 2002. 365–378, 1994. [53] C. Rubin, A. S. Turner, S. Bain, C. Mallinckrodt, and K. McLeod, “Low mechanical signals strengthen long bones,” [36] D. R. Carter and G. S. Beaupre, Skeletal Function and Form, Cambridge University Press, Cambridge, UK, 2001. Nature, vol. 412, no. 6847, pp. 603–604, 2001. [37] L. E. Lanyon and C. T. Rubin, “Functional adaptation in [54] V. Gilsanz, T. A. L. Wren, M. Sanchez, F. Dorey, S. Judex, skeletal structures,” in Functional Vertebrate Morphology,M. and C. Rubin, “Low-level, high-frequency mechanical signals enhance musculoskeletal development of young women with Hildebrand, D. M. Bramble, K. F. Liem, and D. B. Wake, Eds., pp. 1–25, Harvard University Press, Cambridge, Mass, USA, low BMD,” Journal of Bone and Mineral Research, vol. 21, no. 9, pp. 1464–1474, 2006. [55] J. W. Folkins, “Muscle activity for jaw closing during speech,” [38] R. B. Martin, D. B. Burr, and N. A. Sharkey, Skeletal Tissue Mechanics, Springer, New York, NY, USA, 1998. Journal of Speech and Hearing Research, vol. 24, no. 4, pp. 601–615, 1981. [39] L. E. Lanyon and C. T. Rubin, “Static vs dynamic loads as an [56] K. M. Hiiemae and J. B. Palmer, “Tongue movements in influence on bone remodelling,” Journal of Biomechanics, vol. 17, no. 12, pp. 897–905, 1984. feeding and speech,” Critical Reviews in Oral Biology and Medicine, vol. 14, no. 6, pp. 413–429, 2003. [40] H. M. Frost, “Bone “mass” and the “mechanostat”: a [57] M. Kumada,R.T.Todd, F. Bell-Berti,M.Niitsu,H.Hirose, proposal,” Anatomical Record, vol. 219, no. 1, pp. 1–9, 1987. and S. Niimi, “Functions of the muscles of the tongue during [41] C. T. Rubin and L. E. Lanyon, “Regulation of bone mass by speech,” Journal of the Acoustical Society of America, vol. 104, mechanical strain magnitude,” Calcified Tissue International, no. 3, pp. 1819–1820, 1998. vol. 37, no. 4, pp. 411–417, 1985. [58] C. F. Ross, D. A. Reed, R. L. Washington, A. Eckhardt, F. [42] C. T. Rubin, K. J. McLeod,T.S.Gross, andH.J.Donahue, Anapol, and N. Shahnoor, “Scaling of chew cycle duration “Physical stimulus as potent determinants of bone morphol- in primates,” American Journal of Physical Anthropology, vol. ogy,” in Bone Biodynamics in Orthodontic and Orthopedic 138, no. 1, pp. 30–44, 2009. Treatment,D.S.Carlson andS.A.Goldstein, Eds.,pp. 75– 91, University of Michigan Center for Human Growth and [59] C. Lassauzay, M. A. Peyron, E. Albuisson, E. Dransfield, and A. Woda, “Variability of the masticatory process during Development, Ann Arbor, Mich, USA, 1991. chewing of elastic model foods,” European Journal of Oral [43] Y. F. Hsieh and C. H. Turner, “Effects of loading frequency on Sciences, vol. 108, no. 6, pp. 484–492, 2000. mechanically induced bone formation,” Journal of Bone and [60] D. J. Ostry and J. R. Flanagan, “Human jaw movement in Mineral Research, vol. 16, no. 5, pp. 918–924, 2001. mastication and speech,” Archives of Oral Biology, vol. 34, no. [44] D. J. Daegling, “The relationship of in vivo bone strain 9, pp. 685–693, 1989. to mandibular corpus morphology in Macaca fascicularis,” [61] E. Fosler-Lussier and N. Morgan, “Effects of speaking rate Journal of Human Evolution, vol. 25, no. 4, pp. 247–269, 1993. and word frequency on pronunciations in conversational [45] D. M. Cullen, R. T. Smith, and M. P. Akhter, “Bone-loading speech,” Speech Communication, vol. 29, no. 2, pp. 137–158, response varies with strain magnitude and cycle number,” Journal of Applied Physiology, vol. 91, no. 5, pp. 1971–1976, [62] H. Kuwabara, “Acoustic and perceptual properties of phonemes in continuous speech as a function of speaking [46] M. R. Forwood and C. H. Turner, “The response of rat tibiae rate,” in Proceedings of the 5th European Conference on Speech to incremental bouts of mechanical loading: a quantum Communication and Technology (EUROSPEECH ’97 ),pp. concept for bone formation,” Bone, vol. 15, no. 6, pp. 603– 1003–1006, Rhodes, Greece, 1997. 609, 1994. [63] M. A. Levent and H. L. H. John, “A study of temporal features [47] J. E. A. Wolff, “A theoretical approach to solve the chin and frequency characteristics in American English foreign problem,” in Food Acquisition and Processing in Primates,D.J. accent,” Journal of the Acoustical Society of America, vol. 102, Chivers, B. A. Wood, and A. Bilsborough, Eds., pp. 391–405, no. 1, pp. 28–40, 1997. Plenum Press, New York, NY, USA, 1984. Journal of Anthropology 13 [64] N. Morgan and E. Fosler-Lussier, “Combining multiple modern human molars,” Journal of Human Evolution, vol. 55, estimators of speaking rate,” Acoustics, Speech and Signal no. 1, pp. 12–23, 2008. Processing, vol. 2, pp. 729–732, 1998. [83] K. Kupczik and J. J. Hublin, “Mandibular molar root [65] T. W. P. Korioth, D. P. Romilly, and A. G. Hannam, “Three- morphology in Neanderthals and Late Pleistocene and recent dimensional finite element stress analysis of the dentate Homo sapiens,” Journal of Human Evolution,vol. 59, no.5,pp. human mandible,” American Journal of Physical Anthropol- 525–541, 2010. ogy, vol. 88, no. 1, pp. 69–96, 1992. [84] E. K. Sauerland and S. P. Mitchell, “Electromyographic [66] M. Motoyoshi, Y. Hama, E. Sugi, K. Takahashi, K. Kamijo, activity of the human Genioglossus muscle in response to and S. Namura, “A finite element model of the human face. respiration and to positional changes of the head,” Bulletin of Stress distribution around the chin due to articulation of the Los Angeles neurological societies, vol. 35, no. 2, pp. 69–73, the five vowels in Japanese,” The Journal of Nihon University School of Dentistry, vol. 38, no. 1, pp. 11–20, 1996. [85] R. C. Basner, J. Ringler, R. M. Schwartzstein, S. E. Weinberger, [67] J. T. Stern Jr., Essentials of Gross Anatomy, FA Davis, and J. Woodrow Weiss, “Phasic electromyographic activity Philadelphia, Pa, USA, 1988. of the genioglossus increases in normals during slow-wave [68] W. L. Hylander, “Stress and strain in the mandibular sleep,” Respiration Physiology, vol. 83, no. 2, pp. 189–200, symphysis of primates: a test of competing hypotheses,” American JournalofPhysicalAnthropology,vol. 64, no.1,pp. [86] E. K. Sauerland and R. M. Harper, “The human tongue 1–46, 1984. during sleep: electromyographic activity of the genioglossus [69] B. Tuller, K. S. Harris, and B. Gross, “Electromyographic muscle,” Experimental Neurology, vol. 51, no. 1, pp. 160–170, study of the jaw muscles during speech,” Journal of Phonetics, vol. 9, pp. 175–188, 1981. [87] R. T. Brouillette and B. T. Thach, “Control of genioglossus [70] H. Fukase, “Functional significance of bone distribution in muscle inspiratory activity,” Journal of Applied Physiology the human mandibular symphysis,” Anthropological Science, Respiratory Environmental and Exercise Physiology, vol. 49, vol. 115, no. 1, pp. 55–62, 2007. no. 5, pp. 801–808, 1980. [71] N. Barber, “The evolutionary psychology of physical attrac- [88] R. F. Fregosi and D. D. Fuller, “Respiratory-related control of tiveness: sexual selection and human morphology,” Ethology extrinsic tongue muscle activity,” Respiration Physiology, vol. and Sociobiology, vol. 16, no. 5, pp. 395–424, 1995. 110, no. 2-3, pp. 295–306, 1997. [72] K. Grammer and R. Thornhill, “Human (Homo sapiens) [89] S. M. Farret, M. Vitti, and M. M. B. Farret, “Electromyo- facial attractiveness and sexual selection: the role of symme- graphic analysis of the mentalis and depressor labii inferior try and averageness,” Journal of Comparative Psychology, vol. muscles in the production of speech,” Electromyography and 108, no. 3, pp. 233–242, 1994. Clinical Neurophysiology, vol. 22, no. 1-2, pp. 137–148, 1982. [73] D. E. Lieberman, “Testing hypotheses about recent human [90] J. Clayton-Smith and L. Laan, “Angelman syndrome: a evolution from skulls: integrating morphology, function, review of the clinical and genetic aspects,” Journal of Medical development, and phylogeny,” Current Anthropology, vol. 36, Genetics, vol. 40, no. 2, pp. 87–95, 2003. no. 2, pp. 159–197, 1995. [91] N. C. Nowlan and P. J. Prendergast, “Evolution of [74] F. Groning ¨ , J. Liu, M. J. Fagan, and P. O’Higgins, “Why do mechanoregulation of bone growth will lead to non-optimal humans have chins? Testing the mechanical signficance of bone phenotypes,” Journal of Theoretical Biology, vol. 235, no. modern human symphyseal morphology with finite element 3, pp. 408–418, 2005. analysis,” American Journal of Physical Anthropology, vol. 144, [92] C. T. Rubin and K. J. McLeod, “Biologic modulation of pp. 593–606, 2011. mechanical influences in bone remodeling,” in Biomechanics [75] I. Ichim, M. Swain, and J. A. Kieser, “Mandibular biomechan- of Diarthrodial Joints,V.C.Mow,A.Ratcliff, and S. L.-Y. Woo, ics and development of the human chin,” Journal of Dental Eds., pp. 97–118, Springer, New York, NY, USA, 1990. Research, vol. 85, no. 7, pp. 638–642, 2006. [93] C. T. Rubin, K. J. McLeod, and S. D. Bain, “Functional strains [76] R. J. Smith, “Categories of allometry: body size versus and cortical bone adaptation: epigenetic assurance of skeletal biomechanics,” Journal of Human Evolution, vol. 24, no. 3, integrity,” Journal of Biomechanics, vol. 23, supplement 1, pp. pp. 173–182, 1993. 43–54, 1990. [77] W. M. Bass, Human Osteology: A Laboratory and Field [94] R. D. Kent, “The uniqueness of speech among motor Manual, Missouri Archaeological Society, Columbia, Mo, systems,” Clinical Linguistics and Phonetics, vol. 18, no. 6–8, USA, 3rd edition, 1987. pp. 495–505, 2004. [78] M. Coquerelle,F.L.Bookstein, andJ.Braga et al., “Sexual [95] C. Rubin, S. Judex, and Y. X. Qin, “Low-level mechanical dimorphism of the human mandible and its association signals and their potential as a non-pharmacological inter- with dental development,” American Journal of Physical vention for osteoporosis,” Age and Ageing,vol. 35, no.2,pp. Anthropology, vol. 145, no. 2, pp. 192–202, 2011. ii32–ii36, 2006. [79] R. L. Costa, Dental pathology and related factors in archaeolog- ical eskimo samples from point hope and Kodiak Island, Alaska, [96] T. M. Cole, “Postnatal heterochrony of the masticatory apparatus in Cebus apella and Cebus albifrons,” Journal of Ph.D. dissertation, University of Pennsylvania, 1977. [80] S. J. Gould and R. C. Lewontin, “The spandrels of San Marco Human Evolution, vol. 23, no. 3, pp. 253–282, 1992. and the Panglossian paradigm: a critique of the adaptationist [97] O. M. Pearson and D. E. Lieberman, “The aging of Wolff ’s programme,” Proceedings of the Royal Society of London B, vol. “law”: ontogeny and responses to mechanical loading in 205, no. 1161, pp. 581–598, 1979. cortical bone,” American Journal of Physical Anthropology, [81] G. S. Krantz, “Sapienization and speech,” Current Anthropol- vol. 39, pp. 63–99, 2004. ogy, vol. 21, no. 6, pp. 773–792, 1980. [98] S. McBrearty and A. S. Brooks, “The revolution that wasn’t: a [82] A. J. Olejniczak, T. M. Smith, R. N. M. Feeney et al., “Dental new interpretation of the origin of modern human behavior,” tissue proportions and enamel thickness in Neandertal and Journal of Human Evolution, vol. 39, no. 5, pp. 453–563, 2000. 14 Journal of Anthropology [99] F. E. Grine and D. J. Daegling, “New mandible of Paranthro- pus robustus from Member 1, Swartkrans Formation, South Africa,” Journal of Human Evolution, vol. 24, no. 4, pp. 319– 333, 1993. [100] P. Brown and T. Maeda, “Liang Bua Homo floresiensis mandibles and mandibular teeth: a contribution to the comparative morphology of a new hominin species,” Journal of Human Evolution, vol. 57, no. 5, pp. 571–596, 2009. [101] J. L. Thompson and B. Illerhaus, “A new reconstruction of the Le Moustier 1 skull and investigation of internal structures using 3-D μCT data,” Journal of Human Evolution, vol. 35, no. 6, pp. 647–665, 1998. [102] P. Bayle, J. Braga, A. Mazurier, and R. Macchiarelli, “Dental developmental pattern of the Neanderthal child from Roc de Marsal: a high-resolution 3D analysis,” Journal of Human Evolution, vol. 56, no. 1, pp. 66–75, 2009. [103] J. Zilhau, D. E. Angelucci, E. Badal-Garcia et al., “Symbolic use of marine shells and mineral pigments by Iberian Nean- derthals,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 3, pp. 1023–1028, [104] B. Demes, J. T. Stern Jr., M. R. Hausman, S. G. Larson, K. J. Mcleod, and C. T. Rubin, “Patterns of strain in the macaque ulna during functional activity,” American Journal of Physical Anthropology, vol. 106, no. 1, pp. 87–100, 1998. [105] B. Demes, Y. X. Qin, J. T. Stern Jr., S. G. Larson, and C. T. Rubin, “Patterns of strain in the macaque tibia during functional activity,” American Journal of Physical Anthropology, vol. 116, no. 4, pp. 257–265, 2001. [106] D. E. Lieberman, J. D. Polk, and B. Demes, “Predicting Long Bone Loading from Cross-Sectional Geometry,” American Journal of Physical Anthropology, vol. 123, no. 2, pp. 156–171, 2004. 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