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Dietary effects on development of the human mandibular corpus.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:615–628 (2011)
Dietary Effects on Development of the Human
Mandibular Corpus
Megan A. Holmes* and Christopher B. Ruff
Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine,
1830 East Monument Street, Baltimore, MD 21205
KEY WORDS
ontogeny; mandible; cross sectional properties; functional adaptation
ABSTRACT
The extent to which the mandibular corpus exhibits developmental plasticity has important
implications for interpreting variation in adult and juvenile mandibular morphology in the archaeological and
paleontological record. Here, we examine ontogenetic
changes in mandibular corpus breadth, rigidity, and
strength in two population samples with contrasting
diets: late prehistoric Tigara from Point Hope, Alaska,
characterized by a very demanding masticatory regime,
and proto-historic Arikara from the Sully Site in South
Dakota, with a less demanding regime. A total of 52 juvenile and 11 adult Tigara, and 32 juvenile and 10 adult
Arikara were included in the study. Juveniles ranged in
age from 1 to 17 years, with good representation of
younger (1–6-year-old) juveniles (20 Arikara, 18 Tigara).
Superoinferior and buccolingual external and cortical
bone breadths of mandibles were measured at the Pm4M1 and M1-M2 junctions using calipers and biplanar radiographs, respectively. An asymmetrical hollow beam
model was employed to reconstruct cross sections and
calculate bending rigidities and strengths in the sagittal
and transverse planes. Among adults, Tigara have
greater transverse corpus width, bending rigidity, and
strength, and ratios of transverse to sagittal dimensions
than Arikara. This shape difference develops gradually
during growth, with only weak trends among young
juveniles, increasing to near-adult contrasts among adolescents. These results support a role for functional mechanical loading of the mandible during growth in producing adult differences in mandibular corpus morpholV 2011
ogy. Am J Phys Anthropol 145:615–628, 2011.
Variation in mandibular morphology has long been
related to variation in masticatory loadings (e.g.,
Hylander, 1977, 1979; Bouvier, 1986; Daegling, 1989;
Biknevicius and Ruff, 1992a; Ravosa, 1996); based on
this, albeit complex relationship (Daegling, 2007), differences in mandibular form are often used to infer dietary
differences between past species or populations of the
same species (e.g., Carlson and Van Gerven, 1979;
Hylander, 1988; Daegling and Grine, 1991; Ravosa,
1996). In this context, one question that arises is to
what extent mandibular morphology reflects developmental plasticity, i.e., a direct growth-related response to
masticatory loadings, rather than (or in addition to) heritable (genetic) variation. The question is important in
that it bears on both broader phylogenetic interpretations of craniofacial morphological variability (e.g.,
Antón et al., 2010), including ontogenetic variability
(e.g., Mallegni and Trinkaus, 1997; Crevecouer et al.,
2010), as well as narrower behavioral reconstructions in
the archaeological record (Larsen, 1997; Paschetta et al.,
2010).
Experimental studies have demonstrated that the
mandible can exhibit developmental plasticity in
response to dietary manipulation, with animals fed
harder diets during growth developing thicker and stronger mandibular corpora (among other changes) (Bouvier
and Hylander, 1981; Lieberman et al., 2004; Organ et
al., 2006). In this respect, the mandibular corpus
behaves in a way analogous to that of long bones subjected to increased mechanical loading during life (Ruff
et al., 2006 and references therein). However, there is
also evidence that some population differences in relative long bone strength may be present very early during
ontogeny (Cowgill, 2010; also see Wallace et al., 2010).
Fukase and Suwa (2008) reported similar findings for
samples of mandibles from prehistoric Jomon and modern Japanese. Adult Jomon mandibular corpora had previously been shown to have thicker cortical bone than
those of modern Japanese, which was interpreted as a
result of a tougher diet among Jomon (Kanazawa and
Kasai, 1998). Fukase and Suwa showed that this was
also true throughout development at the mandibular
symphysis. They concluded that their results ‘‘reject the
hypothesis that bone mass and deployment in the mandibular symphysis are primarily determined by stress
generated by mastication,’’ ‘‘although a common and
coherent pattern of growth-related changes in cortical
bone thickness. . . suggest(s) that mechanical stress has a
significant regulatory role during growth remodeling of
the symphysis’’ (Fukase and Suwa, 2008: 451-452). They
also found that some other, external dimensions of the
mandible, including buccal-lingual breadth of the corpus
and symphyseal height and breadth, were consistently
larger in Jomon mandibles beginning in infancy, suggesting that they were ‘‘manifestations of genetic patterning,’’ (P. 451) rather than a result of environmental influences during development.
C 2011
V
WILEY-LISS, INC.
C
Wiley-Liss, Inc.
*Correspondence to: Megan A. Holmes, Center for Functional
Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 East Monument Street, #301, Baltimore, MD 21205.
E-mail: megholmes@jhmi.edu
Received 21 December 2010; accepted 18 April 2011
DOI 10.1002/ajpa.21554
Published online 23 June 2011 in Wiley Online Library
(wileyonlinelibrary.com).
616
M.A. HOLMES AND C.B. RUFF
The samples studied by Fukase and Suwa (2008)
were, however, relatively small (total preadolescent N
5 20/19 for Jomon/modern), especially in infancy (1–3
years, N 5 4/6). Also, internal bone dimensions were
only measured (using computed tomography) at the
symphysis, not under the tooth rows, and no actual
cross sectional measures of bone strength or rigidity
(second moments of area and section moduli) were calculated. As shown previously (Daegling, 1989; Biknevicius and Ruff, 1992b), external breadths are of only
limited usefulness and accuracy in assessing mechanical characteristics of the mandible, particularly when
the aim is to identify relatively subtle differences.
Structural interpretation of the mandibular symphysis is
also complicated by a number of factors, including variation in mandibular curvature and symphyseal inclination (Hylander, 1984, 1988; Daegling, 2001), neither of
which was assessed in the Fukase and Suwa (2008)
study. In contrast, the more distal mandibular corpus is
relatively straight and may be more easily modeled (and
interpreted) using standard beam theory (Hylander,
1988; Daegling, 1989; Biknevicius and Ruff, 1992a).
Here, we carry out a comparison of cross sectional geometric properties of the distal mandibular corpus in two
growth series derived from populations with contrasting
dietary regimes and adult mandibular morphologies (see
below)—Tigara Inupiats and Arikara Native Americans.
The null hypothesis is that juveniles and adults from
these samples will exhibit the same distinctions in mandibular rigidity and strength. If true, this would support
Fukase and Suwa’s (2008) contention that mandibular
morphology is largely genetically controlled, with little
direct effect of contrasting dietary regimes. Disproving
the null hypothesis would support a role for masticatory
loadings during development in producing variation in
adult mandibular morphology.
MATERIALS AND METHODS
Samples
The populations employed in this study represent two
genetically and regionally distinct groups with contrasting dietary practices. Tigara specimens represent a circum-polar population which occupied Point Hope, Alaska
between 1200 and 1700 A.D (Larsen and Rainey, 1948).
Archaeological and ethnographic data indicate a diet
consisting of dried meats exploited from marine resources such as fish and sea mammals, which would require
heavy masticatory loading for consumption (Rainey,
1941; El-Zaatari, 2008, 2010). In addition, there is evidence that the Tigara population utilized their dentition
as a tool for gripping, stripping, and softening leather
(Merbs, 1968; Costa, 1980). This behavior was also witnessed in the native Alaskan populations during the first
half of the 20th century (de Poncin, 1941). These behavioral observations, as well as other evidence, such as
high frequencies of dental chipping, fracturing, and root
resorption, as well as direct measurements of high bite
forces, have led researchers to treat arctic populations as
an exemplar of adaptation to strenuous masticatory and
paramasticatory forces (Turner and Cadien, 1969;
Hylander, 1977; Scott and Winn, 2010). In fact, these
populations have been repeatedly utilized in comparative
studies involving fossil hominids as they are thought to
emulate in some ways earlier dietary regimes (Hylander,
1988; Spencer and Demes, 1993; Nicholson and Harvati,
2006). They, thus, represent a modern extreme for mastiAmerican Journal of Physical Anthropology
TABLE 1. Sample size for Arikara and Tigara populations
arranged by age group and cross-section location
Pm4-M1
Age (yr)
1–6
6–12
12–18
Adults
Total
M1-M2
Arikara
Tigara
Total
Arikara
Tigara
Total
20
6
6
10
42
18
23
11
11
63
37
29
17
21
105
9
5
6
10
30
5
23
11
11
50
14
28
17
21
80
catory loading. A total of 63 individuals—52 juveniles
and 11 adults—were obtained from the collections of the
American Museum of Natural History (AMNH), New
York (Table 1).
The second comparative sample, Arikara from the
Sully Site, South Dakota, provide a model for a less
strenuous diet. This skeletal population was excavated
from a proto-historic site dating from 1650 to 1750 A.D
(Jantz, 1973; Jantz and Owsley, 1984; Owsley and Jantz,
1985). Seasonal climates allowed for a relatively varied
subsistence strategy that included horticulture and
hunting. Dental wear analyses of protohistoric Arikara
populations also suggest that their diet was mixed, consisting of both plant and animal foods (Ungar and
Spencer, 1999; El Zaatari, 2008). Though the Arikara
are thought to have consumed dried meat like the Tigara
(Ungar and Spencer, 1999), direct comparisons of dental
microwear patterns between these two populations demonstrate their dietary differences, and are consistent
with heavier loading (as well as a more abrasive diet)
among the Tigara (El Zaatari, 2008). It may be gathered
from this information that the Tigara population possessed a diet that included generally higher occlusal
loads and greater masticatory demands relative to that
of the Arikara. A total of 42 individuals—32 juveniles
and 10 adults—were obtained from the collections of the
Smithsonian Institution National Museum of Natural
History (NMNH), Washington, DC.
The growth series utilized here encompass all developmental stages from infancy to adulthood (Table 1 and
subsequent figures). Individuals were aged using a combination of Liversidge and Molleson’s (2004) deciduous
tooth root length regression equations, Smith’s (1991)
dental development sequence, and timing of long bone
epiphyseal fusion among adolescents (Scheuer and
Black, 2000). Those specimens presenting a fully erupted
M3 were considered adults. For discrete age group comparisons, juveniles were organized into three subgroups
demarcated by the eruption of the first two permanent
mandibular molars, roughly coinciding with ages of 6
and 12 years, i.e., 1–6, 6–12, and 12–18 years (Table 1).
No attempt was made to sex pre-adolescents; older adolescents and adults contained an approximately equal
number of male and females in each sample, determined
from pelvic morphology (Buikstra and Ubelaker, 1994),
to control for possible sexual dimorphism. To limit possible effects of tooth loss, tooth wear, and other consequences of aging, adults were limited to individuals between
18 and 28 years, determined using the presence of a
fully erupted M3 and standard postcranial observations
(Buikstra and Ubelaker, 1994). In addition, edentulous
mandibles, mandibles with extensive damage and/or
mandibles that did not meet the requirements for length
measurement were excluded from this analysis. When
available, measurements were preferably taken on the
GROWTH OF THE HUMAN MANDIBULAR CORPUS
617
TABLE 2. List of measurements and definitions
Abbreviation
ML
Dx
Dy
Iy
Ix
Zy
Zx
Measurement
Definition
Mandibular Length
Corpus Width
Corpus Height
Transverse bending rigidity
Sagittal bending rigidity
Transverse bending strength
Sagittal bending strength
distance from the center of the condyle to the Pm3-C junction
transverse (buccolingual) corpus breadth (mm)
sagittal (superior-inferior corpus breadth (mm)
second moment of area about the sagittal axis (mm4)
second moment of area about the transverse axis (mm4)
section modulus about the sagittal axis (mm3)
section modulus about the transverse axis (mm3)
Fig. 1. Calculation of cross-sectional geometric properties using the asymmetrical hollow beam model. A, B: Buccolingual and
superoinferior radiographs of a juvenile mandible showing corpus height, Dy, and breadth, Dx, taken with calipers on specimens,
and inferior, Ic, lingual, lc and buccal, bc, cortical breadths, measured using ImageJ on digital radiographs, at the Pm1-M1 location.
C: These measurements are then used to calculate total subperiosteal (solid line) and endosteal (dotted line) areas and second
moments of area, as well as the centroid for each (solid x, subperiosteal centroid; dotted x, medullary centroid). D: Subsequently,
cortical area and the composite centroid (x) are calculated, which are then used with periosteal and endosteal properties to calculate
composite second moments of area and section moduli using asymmetrical hollow beam formulae (http://www.hopkinsmedicine.org/
fae/CBR.htm; see Biknevicius and Ruff (1992) and O’Neill and Ruff (2004) for discussion).
right side of the mandible, however, left sides were
measured when necessary to maximize sample sizes.
Measurements
Both linear measurements and cross sectional geometric properties of the mandible were collected for this
study (see Table 2). Linear dimensions, measured using
digital calipers, included mandibular length, measured
from the center of the articular process to the Pm3-C
junction, and corpus height (Dy) and width (Dx), measured perpendicular to the long axis of the mandible in
the sagittal (superoinferior) and transverse (buccolingual) planes, respectively (see Fig. 1). Dx and Dy and
other cross sectional measurements were determined at
two locations, behind dm2 or Pm4 if erupted (Pm4-M1
margin), and behind M1 (M1-M2 margin). Before eruption of dm2 or M1, the developing crowns, when visible
American Journal of Physical Anthropology
618
M.A. HOLMES AND C.B. RUFF
TABLE 3. Comparison of Arikara and Tigara adult mandibular
dimensions
Arikara
Adults
Tigara
Adults
Propertya
Mean
SE
Mean
SE
p-valueb
ML
98.1
1.47
99.9
1.33
0.392
Dx
Dy
Iy
Ix
Zy
Zx
Dx/Dy
Iy/Ix
Zy/Zx
14.9
32.2
3425
9898
304
591
0.465
0.356
0.521
0.42
0.89
254
767
14.9
32.8
0.017
0.025
0.022
18.6
31.5
6273
10689
484
651
0.593
0.587
0.743
0.65
0.68
626
763
33.2
33.3
0.020
0.037
0.029
0.000
0.517
0.001c
0.474
0.000c
0.219
0.000
0.000
0.000
Dx
Dy
Iy
Ix
Zy
Zx
Dx/Dy
Iy/Ix
Zy/Zx
17.3
29.7
4592
8172
364
528
0.581
0.581
0.697
0.36
0.81
220
664
11.9
30.8
0.069
0.046
0.031
20.3
28.6
6854
8025
490
538
0.710
0.855
0.905
0.59
0.52
714
719
43.4
40.6
0.020
0.048
0.031
0.000
0.263
0.011c
0.884
0.017c
0.853
0.000
0.000
Pm4-M1
M1-M2
a
b
c
See Table 2 for property abbreviations.
t tests.
t test with unequal variance applied.
radiographically (see below), were used to locate these
positions. Lack of space behind M1 precluded measurements at this location in some of the youngest individuals (\ 3 years).
Bi-planar radiography, in combination with external
linear measurements, can be used to reconstruct bone
cross sectional geometry (Biknevicius and Ruff, 1992a;
O’Neill and Ruff, 2004). Radiographic digital images
were obtained for each mandible in both the sagittal and
transverse planes, with the superior alveolar border
used to define the long axis of the mandibular corpus.
Specimens collected at the NMNH were digitally radiographed using a Kevex PXS10-16W Microfocus X-Ray
source at 68.9 kV and a PaxScan 4030R Varian System
Flat Panel Amorphous Silicon Digital X-Ray. A portable
Aribex NOMAD handheld X-Ray device (60 kV) and AFP
Digital #2 sensor were utilized to obtain radiographic
digital images of specimens housed at the AMNH.
Cortical thicknesses were measured on the buccal, lingual, and inferior aspects of the mandible on the digital
radiographic images using ImageJ (Abramoff et al.,
2004) (see Fig. 1). Alveolar cortical bone was often too
thin to visualize radiographically; therefore, a thin
straight line (.1 mm thick) was used to complete the alveolar perimeter. The mandibular corpus was modeled
as an asymmetrical hollow beam, which has been shown
to provide a good approximation to true cross sectional
geometry of the corpus (Biknevicius and Ruff, 1992b).
Cross sectional properties were derived using a custom
macro (‘‘EEM_Macro,’’ available at http://www.hopkinsmedicine.org/fae/CBR.htm; also see O’Neill and Ruff,
2004). Biomechanical variables assessed included measures of bending rigidity (I) and strength (Z) in the sagittal (Zx, Ix) and transverse (Zy, Iy) planes. (Note that
rigidities and strengths are measured about, i.e., perpendicular to, the designated axes.) Transverse to supero-inAmerican Journal of Physical Anthropology
ferior ‘‘shape’’ indices were also calculated, from both linear measures (Dx/Dy) and cross sectional parameters (Iy/
Ix; Zy/Zx). These are analogous to traditional mandibular
‘‘robusticity’’ indices (Chamberlain and Wood, 1985; Daegling and Grine, 1991).
Statistical analyses
Mandibular length dimensions are often used as a
mandibular size proxy (Hylander, 1979, 1988; Bouvier,
1986; Biknevicius and Ruff, 1992b; Cole, 1992; Daegling,
2007). To assess whether size standardization was necessary in comparisons between the Tigara and Arikara
samples, we first compared mandibular lengths between
the samples. As shown below, mandibular length is nonsignificantly different between Tigara and Arikara
adults; the two samples are also equivalent in mandibular length in the earliest (1–6 year) age group (66.0 6
1.4 mm (SE) in Tigara; 65.2 6 2.0 mm in Arikara; t 5
0.32; P 5 0.76). Therefore, all comparisons between
groups were carried out using nonsize-standardized
data. This also allows for more direct visualization of
actual growth trajectories. All data (except shape ratios)
were log-transformed in order to normalize distributions
and preserve proportionality over the entire age range
examined.
Adult dimensions were initially compared between the
two samples using t tests, to assess whether significant
differences in morphology existed at the termination of
growth. Because growth itself is nonlinear, however, and
because age distributions of the two samples were not
entirely equivalent, even within the 6-year-age groups
employed, a more complex method was necessary to
carry out ontogenetic comparisons. Polynomial regressions were fit to pooled sample distributions for each
variable, and regression residuals from these lines were
used to compare samples (Pinhasi et al., 2005, 2006;
Mays et al., 2009). The correct order of the polynomials
was determined using a forward step criterion. It was
found that second and third order polynomials matched
growth of the mandibular corpus best for almost all
properties, except for shape ratios at the M1-M2 junction,
which were best fit by linear regressions. Subsequently,
nonstandardized residuals were calculated as each individual’s vertical distance from the predicted pooled
growth trajectory (polynomial line), and used in t tests
between Tigara and Arikara within each of the four developmental age groups (including adults as a group). A
probability value of 0.05 was considered statistically significant in individual comparisons. However, because
multiple comparisons across four groups were employed
here, a Bonferroni correction of 0.05/4 5 0.0125 is appropriate. Both significance levels are indicated in the tabulation of results. Where variances were not equivalent, t
tests with unequal variances were applied.
One additional statistical analysis was also carried
out, again utilizing residuals from the polynomial regressions. ANCOVA was used to compare overall change in
residuals (slope) between the population samples with
increasing age (as a covariate). Significant interaction
terms between population and age indicate divergent
slope trajectories of the residuals, demonstrating divergence in overall growth patterns. A limitation of this
approach is that it fits residuals using a linear model,
whereas population divergences during growth do not
occur at a constant rate (see below). However, because it
GROWTH OF THE HUMAN MANDIBULAR CORPUS
619
Fig. 2. Scatterplots and polynomial regressions on age for each variable, measured at the Pm4-M1 junction. Mandibular breadth
dimensions on left, height dimensions on right. See Table 2 for abbreviations. Filled black circles: Tigara; open triangles: Arikara.
combines information from all age periods, it is a useful
adjunct to the discrete age groups comparisons.
All statistical analyses were carried out using SPSS
ver. 17.0 (SPSS) while Statistica 7.0 (Statsoft) was used
to generate graphical presentations.
RESULTS
Comparisons between the adult sample dimensions
are shown in Table 3. Arikara and Tigara adult mandibles do not differ in mandibular length or corpus height
dimensions (Dy, Ix, Zx) at either the Pm4-M1 or M1-M2
locations. However, Tigara adults are significantly larger
in corpus breadth dimensions (Dx, Iy, Zy) at both loca-
tions. As a consequence, cross sectional ‘‘shape’’ ratios,
Dx/Dy, Iy/Ix, and Zy/Zx, are all significantly greater
among Tigara adults, indicating that they have relatively rounder, more mediolaterally buttressed cross
sections.
Scatterplots and polynomial regressions of mandibular
cross sectional dimensions on age are shown in Figures
2 and 3 for the Pm4-M1 and M1-M2 locations, respectively and for the three shape ratios in Figure 4. Comparisons of residuals from the fitted polynomial curves
in each of the four age categories are shown in Table 4.
Box plots of residuals by age group are given in Figures
5–7 for dimensions measured at Pm4-M1 and M1-M2,
and shape ratios, respectively.
American Journal of Physical Anthropology
620
M.A. HOLMES AND C.B. RUFF
Fig. 3. Scatterplots and polynomial regressions on age for each variable, measured at the M1-M2 junction. Mandibular breadth
dimensions on left, height dimensions on right. See Table 2 for abbreviations. Filled black circles: Tigara; open triangles: Arikara.
No differences between population samples reach statistical significance with Bonferroni correction (p
\0.0125) in the 1–6 year age group (Table 4). Some
breadth dimensions (Dx and Iy) and the three shape indices reach significance at the Pm4-M1 location in noncorrected comparisons (P \0.05), in all cases being greater
in Tigara (Figs. 5A,C and 7A,C,E). No differences reach
significance using either criterion at the M1-M2 location
in the earliest age group.
In the 6–12 year age group, the mandibular strength
ratio, Zy/Zx, at M1-M2 is significantly larger among
Tigara at the Bonferroni-corrected level (Table 4; Fig.
6E). No other comparisons reach this level of significance, although Zy/Zx at Pm4-M1, Dx/Dy (both locations)
American Journal of Physical Anthropology
and Iy/Ix (M1-M2) are significant at the uncorrected level
(all larger in Tigara) (Fig. 7A,C,D).
All of the shape ratios become highly significantly different (p .003) between samples during adolescence
(12–18 years), in all cases being larger in Tigara (Table
4; Fig. 7). Mandibular external height (Dy) is significantly greater among Arikara adolescents, reaching the
Bonferroni-corrected level at M1-M2 (Fig. 6B), and the
uncorrected level at Pm4-M1 (Fig. 5B). Differences
among adults in polynomial residuals parallel those
observed earlier using simple t tests (Table 3).
Direct comparisons of individual data points and box
plots of age group distributions for shape ratios (Figs. 4
and 7) clearly demonstrate the increasing contrast in
GROWTH OF THE HUMAN MANDIBULAR CORPUS
621
Fig. 4. Scatterplots and polynomial regressions on age for shape ratios, measured at the Pm4-M1 (left) and M1-M2 (right) junctions. See Table 2 for abbreviations. Filled black circles: Tigara; open triangles: Arikara.
cross sectional shape between Tigara and Arikara that
develops throughout ontogeny and which characterizes
adults. There is extensive overlap in shape between the
populations early in development, but by adolescence
they are almost completely nonoverlapping. This is
mainly due to relatively greater increases in mandibular
breadth dimensions among Tigara, although a transient
increase in relative height among Arikara also contributes during adolescence (Figs. 2, 4, 5, and 6). Both samples demonstrate a progressive increase during development in relative parasagittal bending rigidity and
strength at both locations (Figs. 2–4).
These observations are corroborated by the ANCOVA
results for regression residuals on age (Table 5). The
external breadth (Dx/Dy) and strength (Zy/Zx) ratios at
both mandibular locations show significant populationage interactions, reflecting the increasing divergence of
values between samples with age. As expected for these
residual analyses, there are no age effects. There is a
marginally significant (p 5 0.047) effect of population on
the Iy/Ix rigidity ratio, only at the Pm4-M1 location.
DISCUSSION
Mandibular corpus morphology is clearly distinct in
adult Tigara and Arikara, with Tigara exhibiting significantly more mediolaterally buttressed corpora mesial
and distal to M1. This is evident in both external linear
American Journal of Physical Anthropology
622
M.A. HOLMES AND C.B. RUFF
TABLE 4. Results of t tests (p-values) between population residuals from polynomial regressions at each age interval. Individually
significant results (p < 0.05) are italicized
Pm4-M1
M21-M2
Propertya
1–6 yr
6–12 yr
12–18 yr
Adults
1–6 yr
6–12 yr
12–18 yr
Adults
Dx
Dy
Iy
Ix
Zy
Zx
Dx/Dy
Iy/Ix
Zy/Zx
0.019
0.914
0.047
0.544
0.091
0.521
0.040
0.026
0.024
0.291
0.089
0.891
0.181
0.982
0.168
0.027
0.051
0.013
0.031
0.016b
0.563
0.066
0.823
0.089
0.000*
0.000*
0.000*
0.000*
0.193
0.001*
0.801
0.000*
0.454
0.000*
0.000*
0.000*
0.544
0.143
0.399
0.266
0.382
0.451
0.742
0.327
0.515
0.091
0.150
0.789
0.029
0.283
0.023
0.014
0.022
0.011*
0.142
0.003*,b
0.252
0.004*
0.070
0.005*
0.002*
0.002*
0.003*
0.000*
0.092
0.017
0.667
0.029b
0.984
0.000*
0.000*
0.000*
All data, except ratios, are log-transformed.* p-values meet Bonferroni correction level (p \ 0.0125).
See Table 2 for abbreviations.
t test with unequal variance applied.
a
b
Fig. 5. Boxplots of residuals from polynomial regressions for dimensions measured at the Pm4-M1 junction (see Fig. 2) for four
age groups in Arikara (open) and Tigara (shaded). See Table 2 for abbreviations.
American Journal of Physical Anthropology
GROWTH OF THE HUMAN MANDIBULAR CORPUS
623
Fig. 6. Boxplots of residuals from polynomial regressions for dimensions measured at the M1-M2 junction (see Fig. 3) for four
age groups in Arikara (open) and Tigara (shaded). See Table 2 for abbreviations.
dimensions, as well as measures of rigidity and strength
that also take into account cortical bone thickness and
distribution. This morphological distinction is not simply
a result of size differences between the populations,
mandibular length is equivalent, as are mandibular
height and sagittal rigidity and strength dimensions.
This shape difference, most clearly expressed as ratios
between buccolingual and sagittal dimensions, progressively develops throughout ontogeny. There is a slight
tendency, not statistically significant by more stringent
multiple-group comparison criteria, for individuals in
our youngest age group, 1–6 years, to exhibit this difference at the Pm1-M1, but not M1-M2 location. However,
the difference between groups becomes much more
marked in older age groups, reaching adult levels of sig-
nificance by adolescence. This is also indicated by the
significant population-age interaction terms for external
breadth and strength ratios at both mandibular locations. The shape difference among adolescents and
adults is mainly a result of greater growth in buccolingual dimensions among Tigara.
Thus, like Fukase and Suwa (2008) and others
(Carlson and Van Gerven, 1977; Spencer and Demes,
1993; Antón et al., 2010), we find that adults from populations with contrasting dietary regimes exhibit differences in mandibular morphology. However, unlike Fukase
and Suwa (2008), we find much less evidence for such
differences among the youngest juveniles from the same
populations, who are much less clearly differentiated
than older juveniles and adults. Thus, our results sugAmerican Journal of Physical Anthropology
624
M.A. HOLMES AND C.B. RUFF
Fig. 7. Boxplots of residuals from polynomial regressions for shape ratios measured at the Pm4-M1 and M1-M2 junction (see Fig.
4) for four age groups in Arikara (open) and Tigara (shaded). See Table 2 for abbreviations.
gest that functional adaptation of the mandible to masticatory loading during growth and development may contribute to the ultimate morphological differences characteristic of adults.
The contrast in results between our study and those of
Fukase and Suwa (2008) may be in part attributable to
the different mandibular dimensions sampled, as well as
the available sample sizes. As noted earlier, biomechanical interpretation of symphyseal morphology, the main
focus of the Fukase and Suwa study, is potentially more
difficult than that of the midcorpus region sampled here
(Hylander, 1984, 1988; Daegling, 2001). It is interesting
American Journal of Physical Anthropology
in this regard that Fukase and Suwa found no differences in symphyseal bending rigidities between their adult
Jomon and modern Japanese samples (their data also
imply no difference in torsional rigidity), despite differences in absolute and relative cortical thicknesses. We
also had available a larger total sample of juveniles (N
5 83 vs. 54 in the Fukase and Suwa study), particularly
in the youngest age ranges (N 5 37 vs. 23 for 1–6 years,
N 5 21 vs. 10 for 1–3 years). This allowed fitting of
more realistic nonlinear growth curves to the data, as
well as more direct comparisons of dimensions within
specific age groups, whereas the Fukase and Suwa study
GROWTH OF THE HUMAN MANDIBULAR CORPUS
TABLE 5. ANCOVA results (p-values) for residuals from
polynomial regressions on age
Pm4-M1
M1-M2
Propertya Population Age Pop*age Population Age Pop*age
Dx
Dy
Iy
Ix
Zy
Zx
Dx/Dy
Iy/Ix
Zy/Zx
0.433
0.975
0.448
0.796
0.566
0.831
0.176
0.047
0.079
0.671
0.851
0.828
0.904
0.839
0.928
0.705
0.847
0.719
0.003
0.158
0.153
0.326
0.170
0.458
0.014
0.366
0.027
0.769
0.827
0.934
0.682
0.988
0.832
0.641
0.930
0.679
0.894
0.888
0.965
0.899
0.976
0.931
0.766
0.898
0.898
0.029
0.076
0.469
0.165
0.657
0.307
0.016
0.055
0.025
Significant results (p \ 0.05) are italicized. All data, except
ratios, are log-transformed.a See Table 2 for abbreviations.
relied on comparisons of estimated y intercepts (i.e.,
downwardly extrapolated birth values) based on linear
regressions on age in 1–8-year-olds.
It is also possible that the difference in results
between the two studies is due at least in part to greater
genetic differentiation between Fukase and Suwa’s samples than in ours. That is, Jomon and modern Japanese
may have evolved different patterns of mandibular
growth, beginning prenatally, in response to long-term
dietary (or other) selection, whereas Tigara and Arikara
did not. Comparisons of ontogenetic trajectories among
other population samples, particularly biologically
related populations experiencing known changes in dietary patterns, would help to further clarify this issue.
A potentially confounding effect on group comparisons
in either the Fukase and Suwa (2008) or present studies
is the possibility of unaccounted for sexual dimorphism in
mandibular morphology in juvenile samples. The Fukase
and Suwa study included only males in their adult samples, whereas all of their Jomon and some modern Japanese juveniles were not sexed. We included an approximately equal number of adult and older adolescent males
and females, but could not sex younger juveniles. If any of
the juvenile samples included an unbalanced sex distribution, this could have affected age trends if sexual dimorphism of the mandible exists among juveniles. Some earlier studies did in fact report sexual dimorphism in certain
features of the mandible in young children (Schutkowski,
1993; Loth and Henneberg, 2001), although these results
were later questioned (Coqueugniot et al., 2002; Scheuer,
2002). Recent morphometric studies indicate that very little sexual dimorphism of the mandible exists after early
infancy and before midadolescence (Franklin et al., 2007;
Coquerelle et al., in press). Thus, this factor is unlikely to
bias growth studies of mixed-sex samples in this age
range. Inclusion of only adult males in the Fukase and
Suwa (2008) samples, however, introduces a potential
effect on the adult comparisons in that sexual dimorphism
of the mandible is marked among adults, particularly in
areas such as the chin (e.g., Buikstra and Ubelaker, 1994;
Thayer and Dobson, 2010); thus, population-level differences in symphyseal morphology may be greater or less
within single-sex rather than mixed-sex samples.
The development of a rounder, more buccolingually
buttressed posterior mandibular corpus among Tigara
suggests that their mandibles were better adapted to
resist torsional loadings than were those of the Arikara
(Hylander, 1988; Daegling and Grine, 1991). Although
several factors can influence the magnitude of such loadings, powerful masticatory forces are among the most
625
important (Hylander, 1988; Daegling and Grine, 1991).
Overall craniofacial morphology in Inupiat and Inuit populations is consistent with the generation of high bite
forces, both anteriorly and posteriorly (Hylander, 1977;
Spencer and Demes, 1993), as are direct behavioral observations of these populations (see above). Although ontogenetic analyses of these general structural and behavioral
characteristics have not, to our knowledge, been carried
out among these populations, it seems plausible that
young children would not have been exposed to the same
levels of masticatory stress (even scaled for body and/or
mandibular size) as adults. This certainly would have
been the case for young infants who had not yet transitioned to adult diets. Weaning age among recent Alaskan
Inupiats has been estimated to be about 3–4 years
(Chance, 1990). Use of the teeth for paramasticatory functions, i.e., as tools (Merbs, 1968; Costa, 1980), would also
likely have become common only after early childhood.
Eruption and occlusion of the adult dentition itself,
between 6 and 12 years, may have been necessary to
transmit high masticatory loadings (although teeth of
Native arctic populations are not relatively large;
Hylander, 1977). All of these general timing factors would
have applied to Arikara as well as Tigara; the fact that
the two populations diverge in morphology during growth
is indicative of progressive functional (mechanical) differentiation within this common developmental framework.
Previous authors have emphasized the increase in parasagittal bending strength or height of the mandibular corpus in Native arctic samples (Hylander, 1977; Antón et al.,
2010), which we did not find here (in comparison to Arikara). However, Hylander (1977) based his conclusions on
a compilation by Hrdlicka (1940), which did not include
mandibular corpus breadth, so it is not possible to assess
whether that may have been even more increased in the
arctic samples. Furthermore, examination of Hrdlicka’s
original data shows that while one particular ‘‘Eskimo’’
sample (from Kodiak Island) had a large mandibular corpus height, ‘‘Eskimos, in general’’ fall well within the
range, and even slightly below the median, of the other
populations sampled, which were world-wide in distribution. Thus, there is no evidence that they had particularly
large corpus heights. Antón et al. (2010) also emphasized
the increased parasagittal bending rigidity among their
‘‘Alaskan’’ samples, but bending rigidities were only calculated for an Aleut sample, not their Inupiat sample from
Point Hope. Their Point Hope sample had the largest corpus breadth and breadth/height ratio of any of their Holocene samples (the Aleuts were also comparatively high).
In pairwise comparisons, corpus breadth showed more significant differences between Point Hope and other samples
than corpus height (the same was true for Aleuts). Therefore, it appears that this Inupiat sample also exhibits a
relatively rounder, i.e., buccolingually buttressed mandibular corpus. It is also worth noting that the present study
comparison of Tigara was with another population sample,
the Arikara, that was also likely subjected to fairly heavy
masticatory loading, at least in comparison with Western
industrialized populations (see above). Thus, it may not be
surprising that parasagittal bending rigidity and strength
were not increased in Tigara relative to Arikara. In
Hrdlička’s (1940) tabulation, US whites show considerably
lower corpus heights than almost all of his other samples,
including ‘‘Eskimos’’ and several lower latitude Native
American samples.
In addition to biomechanical factors, spatial requirements for the developing dentition have also been sugAmerican Journal of Physical Anthropology
626
M.A. HOLMES AND C.B. RUFF
gested to exert an influence on mandibular size and
shape (Wolpoff, 1975; Wood, 1978; Smith, 1983). Thus, it
is possible that the relatively larger buccolingual
breadth of the mandible in the Tigara sample may be
the result of relatively wider buccolingual molar dimensions. Although there is no doubt that dental size may
directly affect mandibular size, it is unlikely that this
factor explains population differences in corpus shape
between the Arikara and Tigara. First, previous comparative analyses have found little support for a direct relationship between molar width and distal mandibular corpus ‘‘robusticity’’ (breadth/height) (Daegling and Grine,
1991; Plavcan and Daegling, 2006). Second, there is no
evidence that Inupiats and Inuits in general had particularly large molar dimensions when compared with other
Native American groups, including Arikara. The lack of
an increase in dental size among ‘‘Eskimos’’, despite evidence for increased mandibular robusticity, has been
specifically remarked upon by Hawkes (1916) and
Hylander (1972, 1977). The average M1 mesiodistal and
buccal-lingual breadths of a series of 22 ‘‘Eskimo’’ population samples reported by Mayhall (1967) and Turner
(1967) were 11.66 mm and 11.20 mm, respectively, very
similar (especially buccal-lingual) to those measured for
Arikara by Perzigian (1975): 11.54 mm and 11. 22 mm,
respectively (sexes combined in both groups). Falk and
Corruccini (1982) reported similar results for M1
breadths of Point Hope ‘‘Eskimos’’ compared with those
of several other modern human groups. Thus, differences
in dental size per se should not account for the differences in mandibular morphology that we found here.
Our results also have some broader implications
regarding the interpretation of mandibular form in earlier hominins, including among juvenile specimens. If at
least some aspects of mandibular morphology are dependent on functional stimuli during development, then
this implies that such characteristics may be less useful
as phylogenetic markers (e.g., see discussion in Lieberman, 1996; Antón et al., 2010). In this study sample,
this appears to apply to relative mandibular corpus rigidity and strength in buccolingual vs. parasagittal
planes, a commonly noted distinction between different
hominin taxa (e.g., Chamberlain and Wood, 1985;
Hylander, 1988; Daegling and Grine, 1991). In this
respect, it is interesting that even young juvenile Neandertal mandibles appear to express an increase in relative corpus breadth (for their age) compared with modern humans, as do adult Neandertals (Mallegni and
Trinkaus, 1997; Crevecouer et al., 2010, Walker et al.,
2010). It is, of course, likely that a combination of
genetic and environmental effects operate during development to produce final adult mandibular form. As with
all skeletal elements, genetic selection may favor
changes in relative strength (robusticity) of the mandible
under appropriate environmental conditions (Cole, 1992;
Cowgill, 2010; Wallace et al., 2010). However, here we
find that adult differences in mandibular morphology
between two modern human populations with distinct
but not extremely different masticatory loading regimes,
Tigara and Arikara, appear to develop only after the initiation of adult patterns of masticatory behavior.
CONCLUSIONS
Tigara and Arikara adults differ in mandibular corpus
morphology measured at the Pm4-M1 and M1-M2 junctions, with Tigara mandibles exhibiting greater buccolinAmerican Journal of Physical Anthropology
gual bending rigidity and strength, measured radiographically. This structural difference develops throughout growth of the mandible, with very young juveniles
(1–6 years) exhibiting a weak, statistically nonsignificant
difference at Pm4-M1 only, older juveniles (6–12 years)
exhibiting more consistent differences at both locations,
and adolescents (12–18 years) an almost fully developed
adult pattern. The greater rigidity and strength of the
mandibular corpus among older juvenile and adult
Tigara is likely related to their very demanding masticatory and para-masticatory regime. The progressive development of these features supports a role for functional
adaptation of the mandible to applied mechanical loadings during growth.
ACKNOWLEDGMENTS
The authors would like to thank David R. Hunt
(NMNH) and Giselle Garcia-Pack (AMNH) for access to
the collections used in this study; and the Fishes Department (NMNH) for use of their digital X-ray machine. We
are grateful to Evan M. Garofalo for all her assistance in
sexing and aging of specimens. We also thank the
reviewers and Associate Editor for insightful comments
that helped improve this article.
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