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Morphological variation is a result of interplay among multiple intervening factors. For hyoid bones, the shape and size differences have been scarcely covered in the literature and in majority limited to studies of sexual dimorphism or age dependency. To our knowledge, the human hyoid bone, in complete opposite to other cranial bones, has not been fully utilized to address developmental questions in terms of asymmetry or modularity. In the present paper, we used landmark-based methods of geometric morphometrics and multivariate statistical approach to study human hyoid morphology represented by the hyoid body and greater horns in a sample of 211 fused and non-fused bones. Within a sample variation analysis, we showed that the hyoid bone is, by nature, asymmetrical bone which exhibits both directional and fluctuating types of asymmetry and is composed of well-integrated anatomical elements for which the biomechanical load of attached muscles is the most determining factor of variation. Yet, the covariance and evidence of unequal amount of fluctuating asymmetry among modules suggests a certain degree of independence during early stages of development.
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Int. J. Morphol.,
32(1):251-260, 2014.
The Asymmetry and Modularity of the Hyoid Bone
Asimetría y Modularidad del Hueso Hioides
Petra Urbanová*; Petr Hejna**; Lenka Zátopková** & Miroslav Sˇafr**
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol.,
32(1):251-260, 2014.
SUMMARY: Morphological variation is a result of interplay among multiple intervening factors. For hyoid bones, the shape
and size differences have been scarcely covered in the literature and in majority limited to studies of sexual dimorphism or age dependency.
To our knowledge, the human hyoid bone, in complete opposite to other cranial bones, has not been fully utilized to address developmental
questions in terms of asymmetry or modularity. In the present paper, we used landmark-based methods of geometric morphometrics and
multivariate statistical approach to study human hyoid morphology represented by the hyoid body and greater horns in a sample of 211
fused and non-fused bones. Within a sample variation analysis, we showed that the hyoid bone is, by nature, asymmetrical bone which
exhibits both directional and fluctuating types of asymmetry and is composed of well-integrated anatomical elements for which the
biomechanical load of attached muscles is the most determining factor of variation. Yet, the covariance and evidence of unequal amount
of fluctuating asymmetry among modules suggests a certain degree of independence during early stages of development.
KEY WORDS: Hyoid bone; Asymmetry; Modularity; Geometric morphometrics.
INTRODUCTION
In the literature, the hyoid bone is a rather neglected
structure of the human skeleton which has not been given
sufficient attention. Functionally, the hyoid bone serves as
an attachment of supra- and infra-hyoid muscles taking part
in mastication and swallowing. Anatomically, the bone
consists of five elements, an unpaired body, and pairs of
greater and lesser horns. All elements originate in
cartilaginous tissue of the pharyngeal (also known as
brachial) arches. By a generally accepted concept of origin,
the lesser horns and superior part of the body above the ver-
tical ridge are derived from the second, so-called hyoid arch,
while the rest of the body and greater horns differentiate
from the third pharyngeal arch (Scheuer & Black, 2000).
Previous morphological studies of the hyoid bone
focused primarily on describing general shape and size
variations (Pollanen & Ubelaker, 1997; Miller et al., 1998).
It has been noted that size and shape is modified by functional
demands and is affected by the individual’s sex (Kindschuh
et al., 2010), age (Gupta et al., 2008; Urbanová et al., 2013a),
ancestry (Kindschuh et al., 2010; Kindschuh et al., 2012)
and to a lesser extent by body size parameters (Urbanová et
al., 2013b).
Like most human skeletal structures, the hyoid bone
is generally assumed to be bilaterally symmetrical. The left-
right symmetry of hyoid bones corresponds to object
symmetry, where a single structure is identical according to
a given or selected plane, such as mid-sagittal plane. The
matching symmetry, in contrast, is referred to in situations
where two separate objects exist as mirror images of each
other (Klingenber et al., 2002).
The disturbances in symmetry and an occurrence of
asymmetry within data might be an indicator of individual
or population-related developmental stress, shed light on
pathological conditions or indicate a relation between
structurally or functionally interacting elements. The
evidence of asymmetry in the human hyoid bone has been
explored in relation to the individual’s sex (Pollanen &
Ubelaker) and body size (Urbanová et al., 2013b). Recently,
symmetry/asymmetry issues have been explored owing to
the geometric morphometrics (GM). GM has been primarily
helpful in standardizing the manner in which the symmetry
is investigated and in separating three different sources of
asymmetry – directional, fluctuating asymmetry and
antisymmetry (Palmer & Strocker, 1986).
* Department of Anthropology, Faculty of Science, Masaryk University, Brno, Czech Republic.
** Institute of Legal Medicine, Medical Faculty of Charles University and University Hospital Hradec Králové, Hradec Králové, Czech Republic.
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Klingenberg (2008) showed that within the concept
of geometric morphometrics studies of asymmetry can be
combined with other morphological issues – modularity and
integrity. While modularity refers to the covariance among
morphological structures that originates in independent
developmental processes, so-called modules, integration, a
counterpart to modularity, is a measure of the interconnection
among parts in order to function as a whole (Klingenberg,
2008). Modules can be defined with respect to genetic,
developmental, functional or evolutionary context. While
studying adult structures, for instance, the modularity allows
extrapolating morphological data to answer a question on
how the traits or parts interacted developmentally. The
magnitude of interactions among modules is customarily
expressed as a function of their covariance. If the true
boundary between modules is weak meaning that two units
in question are reasonably independent, then the degree of
covariance will be accordingly low. In contrast, two modu-
les linked into a strongly interrelated system will provide a
higher value of covariance.
In the present paper we use geometric morphometrics
to quantify the observed degree of asymmetry in the sample
of fused and non-fused human hyoid bone and to identify
those morphological characteristics that are modular and
those that are integrated in the system throughout anatomical,
functional or developmental interactions.
MATERIAL AND METHOD
The studied sample was composed of 211 hyoid bones
extracted from individuals of Czech origin at medico-legal
autopsies. Both fused and non-fused bones were included
in the study. The distribution of sex was slightly skewed
towards males (117:94). The sample was divided into 4 age
groups: less than 30 years, 31 to 50 years, 51 to 70 years and
more than 71 years (Table I). Only adults were incorporated
in the study. The hyoid morphology was described by a set
of 23 landmarks (Fig.1) covering the body and the greater
horns (lesser horns were not incorporated). The Cartesian
coordinates of all 23 landmarks were recorded by
MicroScribe G2LX digitizerwith a bone or a non-fused
element mounted carefully on a handler. The set of Cartesian
coordinates was further standardized by the generalized
Procrustes fitting.
A/symmetry in size. The size of the bones was expressed
as values of the centroid size. The centroid size is a side-
product of the generalized Procrustes fitting and is computed
as the average distance between landmarks and the center
of gravity of a given configuration.
Table I. Age distribution within studied sample.
Fig. 1. Scheme illustrating a set of recorded landmarks: 1 – poste-
rior end of the right greater horn, 2 – medial inferior end of the right
greater horn, 3 - medial superior end of the right greater horn, 4 –
right lateral superior corner of the body, 5 – superior middle point of
the body, 6 – left lateral superior corner of the body, 7 – left lateral
inferior corner of the body, 8 – the most lateral and inferior left
point of the inferior margin, 9 - inferior middle point of the body, 10
– the most lateral and inferior right point of the inferior margin, 11
– right lateral inferior corner of the body, 12 – the most anterior
point of the horizontal ridge located in mid-sagittal plane, 13 – pos-
terior end of the left greater horn, 14 – medial inferior end of the left
greater horn, 15 – medial superior end of the left greater horn, 16 –
lateral (inferior) margin of the right greater horn in the posterior
third, 17 – lateral (inferior) margin of the right greater horn in the
anterior third, 18 – medial (superior) margin of the right greater
horn in the posterior third, 19 – medial (superior) margin of the
right greater horn in the anterior third, 20 – lateral (inferior) margin
of the left greater horn in posterior third, 17 – lateral (inferior) margin
of the left greater horn in anterior third, 18 – medial (superior) margin
of the left greater horn in the posterior third, 19 – medial (superior)
margin of left greater horn in the anterior third.
In order to test object a/symmetry in size, the origi-
nal configuration of 23 landmarks was subdivided into 2
configurations of 13 landmarks each containing a set of
points from only right or left body side (10 for each side)
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
Age category (years) n %
< 30 7 3.32
31-50 29 13.74
51-70 99 46.92
> 70 76 36.02
Total 211 100.000
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plus 3 mid-sagittal landmarks. For each configuration values
of the centroid size was computed and tested against each
other by t-test (directional asymmetry) and paired t-test
(fluctuating asymmetry). Furthermore, the right-to-left scores
(computed as CSR-CSL, where CSR is a value of the centroid
size of the right-sided configuration and CSL is an equivalent
for the left-sided configuration) were tested in respect to
individual’s sex and age categories by t-test and ANOVA. If
test assumptions were not met, non-parametric alternatives
were processed (Mann-Whitney U test, Kruskal-Wallis test).
Matching a/symmetry was explored on a set of greater
horns described by a configuration of 7 landmarks. Two
separated analyses were carried out, one on non-fused bones
only, and the second where the dataset was pooled with sub-
divisions of the total configuration of the fused hyoids. The
directional and fluctuating asymmetry was tested accordingly
to the object asymmetry, i.e., t-test, paired t-test, ANOVA or
non-parametric alternatives.
A/symmetry in shape. In order to explore a/symmetry in
shape of fused bones the variance of the standardized
Cartesian coordinates was sub-divided into two components,
symmetrical and asymmetrical. The symmetrical component
included displacement of unpaired landmarks along the mid-
sagittal axis and averaged right and left paired landmarks
moving in any direction. It is, in fact, the correction for
studying bilateral data if the symmetry/asymmetry is not a
primary focus. The asymmetrical component is qualified as
a difference between the original and the ideally symmetrical
configuration included into the symmetrical component. A
displacement of unpaired landmarks is allowed in the
direction perpendicular to the mid-sagittal axis while paired
landmarks move freely. In addition to the total configuration
of points, a configuration including landmarks of hyoid body
was processed.
Object a/symmetry in the shape of fused hyoid bones
was tested by the Procrustes ANOVA with the specimen’s
ID and side defined as factors. While “ID” effect counts
individual variation throughout the symmetrical component,
“side” effect reflects the directional asymmetry via the
asymmetrical component. A combination of both effects
sums up the fluctuating asymmetry. Fluctuating asymmetry
was expressed by the Procrustes fluctuating asymmetry
scores and tested against sex and age factors by the Mann-
Whitney U test and one-way ANOVA respectively. In
addition to the subset of fused bones, a configuration of body
landmarks (pooled fused and non-fused bones) was
processed in the same manner.
Matching symmetry was examined on a configuration
of 7 landmarks for the greater horns of each body side by
the Procrustes ANOVA. Prior to the analysis left bones were
left-to-right reflected and the Procrustes fit was performed
on a pooled configuration incorporating both right and left
greater horns. As both configurations become detached, their
spatial arrangement in relations to the body and each other
is lost in the process. As a consequence, the approach tests
for asymmetry of the shape per se regardless of their in vivo
orientation and spatial arrangement. Like object symmetry,
this approach enables distinguishing between directional and
fluctuating asymmetry. The mean of the asymmetrical
component was subsequently ascribed to directional
asymmetry, whereas fluctuating asymmetry was expressed
by the Procrustes fluctuating asymmetry scores and variation
in regards to sex, age and fusion was tested by the Mann-
Whitney U test and one-way ANOVA test respectively. Both
fused and non-fused bones were processed.
Modularity. To localize boundaries in the hyoid bones, the
total configuration of 23 landmarks was divided into a variety
of subsets and treated as separate modules. Only fused bones
were processed. Three main hypotheses were tested:
covariance of true anatomical elements (i.e. greater horns
and body), covariance of compartments of identical
embryonic origin (greater horns, upper and lower parts of
the body) and covariance of superior and inferior halves
(Table III). The extent of covariance was expressed in terms
of the RV coefficient. The assumption was that the covariance
between true modules should be lower than between other
theoretically possible alternative partitions of the same
number of landmarks. Alternatively, if the hyoid bone forms
a single homogeneous module, then all subsets throughout
the bone should co-vary with one another. The probability
of the RV coefficient was acquired by permutation test with
an arbitrary number of 10 000 repeats. Only landmarks
forming a continuous shape were allowed to form random
configurations. Both symmetrical and asymmetrical
components were processed.
The Procrustes fit and most of the statistics were
executed by using MorphoJ software (Klingenberg, 2011).
Additional 3D graphics were prepared with the help of
Landmarks software. For statistical analyses which are not
incorporated into MorphoJ software, Statistica 9 was used.
Assumptions for statistical tests were tested by the Shapiro-
Wilk’s (normality) and Levene’s tests (homogeneity of
covariance matrices). For all tests, statistical significance
was demarcated at the 5% level.
RESULTS
Prior to analysis processing the repeatability of data
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
254
acquisition was tested upon a subsample of 25 bones, selected
randomly from fused bones only. The measurement error
was computed by the Procrustes ANOVA of shape variables
design (Klingenberg & McIntyre, 1998) and by two-way
ANOVA for size variable (centroid size) with individuals
and number of digitizing session as factors. The individual
amount of variation exceeded the digitalization error by
substantial amount (data not shown) suggesting than for
this study, digitalization error is not a concern.
A/symmetry in size
Object a/symmetry. Neither independent nor paired t-test
showed statistically significant in centroid size between
configuration of right and left body landmarks (t= -0,765;
p-value=0.44). Similarly, no connections suggesting
dependency of individual size asymmetry were revealed for
individual’s sex (t-test, t=0.598; p-value=0.55) or age
categories (ANOVA, p-value=0.891).
Fig.e 2. Superimposition of ideally symmetrical hyoid bone (orange) and hyoid of mean asymmetry (blue).
Fig. 3. Superimposition of ideally symmetrical hyoid body (orange) and body of mean asymmetry (blue) and right-left
asymmetrical greater horn (blue) and average right greater horn (orange).
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
255
Matching a/symmetry, greater horns, fused and non-
fused bones (n=211). ANOVA showed statistically
significant differences for directional asymmetry in size of
greater horns if fused and non-fused bones are pooled (Table
III). Right body side possesses larger greater horns than the
left body side. Similarly, statistically significant individual
differences in size were revealed (paired t-test, t=3.818, p-
value=0.0002). Similarly to object a/symmetry no
interactions with individual’s sex (t-test, t=0.547, p-
value=0.585), age categories (ANOVA, p-value=0.924) or
occurrence of fusion (Mann-Whitney U test, U=-0.628, p-
value=0.530) were observed.
Matching a/symmetry, greater horns, non-fused bones
(n=45). The analysis provided comparable results when
narrowed to non-fused bones only, i.e., on average larger
greater horns on the right body side and statistically
significant differences for a pair-wise comparison. However,
sex-related differences were revealed for signed right and
left differences where female bones exhibit, on average,
larger values. If absolute value of side differences (unsigned
scores) were tested, no sex-related differences were observed.
Similarly, non-parametric comparison among age categories
did not show age-dependency (Kruskal-Wallis test, H=3.644,
p-value=0.303).
A/symmetry in shape
Object a/symmetry. Procrustes ANOVA yielded
statistically significant results for asymmetry in the overall
shape as well as the body. Based on a subsample of fused
bones, the mean asymmetry was manifested in unequal
sloping of the greater horns. On average, the right greater
horns tend to curved inwards and upwards whereas the left
greater horns direct down and laterally (Figs. 2 and 4). There
is also an unequal extent of vertical flattening in the right
and left greater horns as the left side tend to flatten to a
larger degree. At the same time, the right half of the infe-
rior margin of the body extended anteriorly, caudally and
laterally (Figs. 3 and 4). The same applies for the asymmetry
analysis of the body configurations (n=211). Furthermore,
an uneven distance between superior and inferior points of
the lateral margin was also a source of right-left asymmetry
(Figs. 3 and 4).
No sex-related or age-dependent variation was
observed within fluctuating asymmetry (FA) scores as the
Mann-Whitney U test and ANOVA yielded statistically
insignificant results (data not shown). Significantly higher
FA scores were revealed for the greater horns than for the
body configuration (paired t-test, t=12.75, p-value <0.0001).
Table II. Procrustes ANOVA results for two types of a/symmetry expressed in shape and size variables within
fused bones and separate anatomical elements.
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
Effect SS MS df F P (param.)
Individual 1.689 0.000320 5280 3.08 <0.0001
Side 0.061 0.002047 30 19.71 <0.0001
Shape
Object s ymmetry
Fused bones Ind*Side 0.514 0.000104 4950
Individual 2.989 0.00129 2310 2.39 <0.0001
Side 0.108 0.01204 9 22.19 <0.0001
Shape
Object s ymmetry
Body Ind*Side 1.025 0.00054 1890
Individual 0.00425 0.000020 210 1.64 0.0002
Side 0.00018 0.000180 1 14.58 0.0002
Centroid size (greater horns)
Matching symmetry Ind*Side 0.00260 0.000012 210
Individual 3.659 0.00124 2940 2.08 <0.0001
Side 0.338 0.02416 14 40.31 <0.0001
Shape (greater horns)
Matching symmetry Ind*Side 1.762 0.00060 2940
Individual 0.00010 0.00001 21 1.22 0.3281
Side 0.00003 0.00003 1 7.07 0.0147
Centroid size (non-fused greater
horns)
Matching symmetry Ind*Side 0.00009 0.00001 21
Individual 0.25380 0.00086 294 1.94 <0.0001
Side 0.008281 0.00059 14 1.33 0.1903
Shape (non-fused greater horns)
Matching symmetry Ind*Side 0.13108 0.00045 294
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Matching a/symmetry, greater horns, fused and non-fused bones
(n=211). Statistically significant results in shape were shown for the
directional asymmetry (Table II). The mean difference between right and
left side was demonstrated in the overall width and flattening. Neither
sex-, age- nor fusion-related variations were observed within the FA scores,
as Mann-Whitney U test and ANOVA yielded statistically non-significant
results.
Matching symmetry, greater horns, non-
fused bones (n=45). No statistically
significant differences in directional
asymmetry of non-fused greater horns were
revealed (Table II).
Modularity. Of the 3 hypotheses of
modularity, the lowest RV coefficients were
achieved with modules partitioned with
respect to different embryonic origin. The
symmetrical component yielded consistently
higher RV coefficients than the asymmetrical
component. Minimal values of the RV
coefficient were given by a partition wherein
the body landmarks 5, 9 and 12 were set
separately from landmarks of the inferior (2,
11, 10, 8, 7, 14) and superior margins (4, 6)
(Table III).
Table III. Tested hypotheses of modularity. RV coefficient corresponds to the covariance among the tested modules (*Number of 10 000
partitions considered).
Fig. 4. Asymmetry in the hyoid bone, body and greater horn displayed in color
scale.
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
Hypothesis Partitions Dataset Multi-set
RV P-value
Symmetrical component 0.60528 0.2369
Subset 1: 1 2 3 13 14 15 16 17 18
19 20 21 22 23
Subset 2: 4 5 6 7 8 9 10 11 12 Asymmetrical com ponent 0.4612 0.273 5
Symmetrical component 0.4486 0.1791
Subset 1: 1 2 3 7 8 9 10 11 13 14
15 16 17 18 19 20 21 22 23
Subset 2: 4 5 6 12 Asymmetrical co mponent 0.3215 0.0856
Symmetrical component 0.3680 0.0157
Subset 1: 1 2 3 13 14 15 16 17 18
19 20 21 22 23
Subset 2: 4 5 6 12
Subset 3: 7 8 9 10 11 Asymmetrical co mponent 0.2835 0.0228
Symmetrical component 0.6121 0.2397
Subset 1: 1 2 7 8 9 10 11 13 14
16 17 20 21
Subset 2: 3 4 5 6 12 15 18 19 22
23 Asymmetrical co mponent 0.4046 0.0347
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DISCUSSION
There is an undeniable presence of asymmetry in the
studied sample of hyoid bones. The asymmetry is present in
both the shape and size of the body and greater horns. Miller
et al. noted that in hyoids, the asymmetry is concentrated in
length rather than width measurements. In a paper by Shimizu
et al. (2005), the asymmetry was concentrated in the breadth
of the greater horns. In our sample, the asymmetry was
manifested by the overall size, unequal length, sloping and
curvature of greater horns, deviation of the midline body
tubercle and an uneven course of the inferior body margin.
On average, the hyoid body was more prominent anteriorly
and extended down and outwards on its right side, while the
right greater horn curved up and inwards. In biological studies,
the average asymmetry is customarily ascribed to the
directional asymmetry. The directional asymmetry can be a
product of genotype as well as of lateralization in the muscle
load or other functional demands (Klingenberg et al., 1998).
In humans, the widely known example of directional
asymmetry is laterality observable in the upper and lower
limbs or the size and functions of the brain (Vallortigara et
al., 1999). The most probable explanation for the observed
average asymmetry in hyoid bones is that it results from a
functional imbalance due to side preferences which are
translated into unequal pull of paired muscles on bone. The
hyoid is not in direct contact with any other bone of the
skeleton. Without fixed or joint connection with other bony
structures, the hyoid lacks compensatory mechanisms which
are involved in retaining morphological equilibrium. These
compensatory mechanisms were acknowledged, for instance,
for bones of cranial vault (Ritchsmeier & Deleon, 2009) or
the facial skeleton (Figalová, 1969) where local defects are
compensated by other parts of the structure. Therefore, any
unilateral preference in muscle load would directly modulate
external morphology.
The average asymmetry is more prominent in the
greater horns than in the body. This is consistent with other
studies where features located near the mid-sagittal plane tend
to manifest a lesser degree of asymmetry. On the other hand,
this seems to be irrelevant if a trait is strongly determined by
unilateral functional demands rather than randomly distributed
differences. For instance, Kolesnikov & An (1999) mentioned
a high degree of asymmetry in the nasal aperture and Hanson
& Owsley (1980) declared right-left asymmetry in the fron-
tal sinuses. Both structures occupy areas in the median line
but are misshaped by stronger pressure of the airflow in one
of the airways.
In addition to directional asymmetry, hyoid bones
exhibit a noticeable extent of fluctuating asymmetry.
Fluctuating asymmetry (FA) arises from diminutive
random irregularities in otherwise bilateral development
(Van Valen, 1962). At a population level, they can be
observed as minor physical anomalies equally distributed
on both body sides. Being a product of random acts, FA
and its occurrence have been used as a measure of
developmental instability (Klingenberg & McIntyre). Since
the right and left body side shares identical genetic coding,
any within-individual right-left asymmetry can be ascribed
to environmental impulses. Although this non-genetic basis
of FA is not yet fully understood and is a question of
ongoing disputes (Leamy & Klingenberg 2005), the
fluctuating asymmetry was previously implicated in
malnutrition, living conditions, toxicity, gestational dia-
betes, obesity, smoking or alcoholism during pregnancy
(Kieser et al., 1997; Møller & Swaddle, 1997; Thornhill
& Møller, 1997; Singh & Rosen, 2001). In the present
study, none of the studied factors exhibited an association
with the extent of FA (except for signed right-to-left scores
of centroid size in non-fused greater horns which is likely
due to sampling bias). This applies in particular to an
individual’s sex, which suggests that both sexes are sus-
ceptible to the same extent and that the hyoid bone may be
resistant to the so-called “male-specific maternal
immunoreactivity”, which assumes that a mother’s immune
response to a male foetus increases developmental
instability (Lalumière et al., 1999).
There is a lack of data on asymmetry in early stages
of development of the hyoid bone. Therefore, for now we
can only speculate at what point in an individual’s life
certain types of asymmetry occur. For the facial skeleton,
for instance, the asymmetry reportedly exists from the early
stages in development to elderly ages (Rossi et al., 2003).
Being a product of developmental events, FA in the hyoid
bone should be identically present at birth and then
throughout life. For some of the somatic measurements,
the extent of FA is somehow prone to diminish gradually
by postnatal events (Wilson & Manning, 1996). If valid in
the case of the hyoid bone, we would have observed a
decrease in Procrustes fluctuation scores with advancing
age. No such age-dependent decrease was, however,
yielded. By contrast, the directional asymmetry, being
driven by biomechanical demands, would be expected to
increase with age increment or at least dependency upon
biological sex. Our results failed, again, to confirm that
the asymmetry changes with advancing age or is more
apparent in male bones.
The comparison between the body and greater horns
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
258
revealed that the greater horns are more inclined towards
local disturbances. FA can be used as a tool to study patterns
and amount of integration among anatomical parts in
developmental processes as an uneven extent of FA among
various compartments of the same anatomical structure is
generally taken as an evidence for weaker within
compartment interactions which are then more suscepti-
ble towards effects of environmental factors (Klingenberg
et al., 2002). Given the independent lateral positions of
the greater horns in contrast to the centrally placed single-
structured body it is certainly the case for the human hyoid
bone.
We have shown that methods of geometric
morphometric are very effective in exploring hypotheses
about independency of skeletal units. The mammalian skull
is highly integrated and evolutionary conserved system
(Porto et al., 2009). Still, for the human craniofacial
complex it has been noted that although the intra-module
integration is very high the integration among traditional
anatomical regions such as basicranium, facial skeleton
and cranial vault are loosened in comparison to other
species (Richtsmeier & Deleon).
In regards to our results, there is a clear division of
the hyoid bone into subdivisions, the first is the one that
respects obvious anatomical units and the second, which
was revealed as predominant, is the developmental
compartmentalization due to a different embryonic origin.
Even stronger integration was, however, revealed for the
superior and inferior halves of the bone. Hyoid morphology
is mostly determined by the biomechanical load of the
suprahyoid and infrahyoid muscles. Hence, the
morphology of the body co-varied with that of greater horns
and so did the superior and inferior margins.
The symmetrical components yielded stronger
covariance coefficients in anatomical subdivision as well
as across the remaining tested hypotheses. The weaker
integration of asymmetry is considered a widespread
phenomenon as it was previously reported for other ani-
mal species, such as dogs, rodents or insects (Drake &
Klingenberg, 2010; Klingenberg, 2009).
It has been previously held that the hyoid bone
originates from two embryonic structures. While the su-
perior part of the body together with the lesser horns
originate from the second pharyngeal arch, the greater horn
and inferior part of the body originate from the third
pharyngeal arch. Our results showed that partitions
according to this dichotomy revealed a lower covariance
than when anatomical or topographic elements were
incorporated. This indicates that the superior and inferior
parts of the body are distinct units and developmental
integrations in the bone occur primarily within these units
and not between them. Surprisingly, we were provided with
an alternative scenario of three independent compartments
which yielded the weakest theoretical dependency for all
of the tested partitioning. According to the results, there
appears to be a loosening of the otherwise homogenous
interactions between the lateral parts and midline portion
of the body. Due to a lack of appropriate landmarks on a
structure, the exact location of the marginline delimiting
these modules remained unresolved.
Recently, the concept of dual origin involving the
second (hyoid) and third pharyngeal arches in the human
hyoid has been questioned. Rodríguez-Vázquez et al.
(2011) demonstrated on embryos that the hyoid body
originates from a mesenchymal condensation that is
separated from the second and third arch at an early stage
of development and subsequently acts as an independent
unit. By this, the hyoid bone would originate from the
second and third pharyngeal arches for the lesser and
greater horns respectively and mesenchymal cells separated
most likely from the hypobrachial eminence “located at
the base of the third pharyngeal arch” (Rodríguez-Vázquez
et al.).
It is unclear whether this could translate to our
results or is simply an unforeseen relict of the analysis.
Certainly further studies are required. For example, patterns
of fluctuating asymmetry within each module and their
correlation could shed light on the extent of developmental
interactions. Two modules will be correlated if there
aredevelopmental interactions between them that can
transmit the effect to both structures, for example, the
presence of a common precursor. If, however, they develop
separately, without any interactions, actions of a stressor
cannot be transmitted (Leamy & Klingenberg).
Unfortunately, there are a limited number of modules that
are suitable for this particular investigation. First of all,
one would have to deal with the technical difficulty
concerning the manner by which the morphology is
described and modules are delimited. Due to ossification
and ongoing bone remodeling in adult skeletal structures,
original embryonic modules are almost impossible to
recognize by an external examination. For hyoid bones,
specifically, it would most likely require a set of additional
reliable landmarks which on a structure like the hyoid bone
are uneasy to define. A collective study involving other
skeletal structures of identical embryonic origin, such as
the styloid process, stapes or thyroid cartilage could be of
help. Furthermore, a study which would incorporate the
lesser horns into the analysis could further elucidate these
interactions.
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
259
CONCLUSION
This study represents a contribution to morphological
studies of the human hyoid bone. In terms of covariance,
the studied anatomical elements, e.g. body and greater horns,
form relatively strongly integrated units. It was demonstrated
that modern analytical tools can provide an insight to patterns
of this integration. The modularity and asymmetry analyses
demonstrated that, by taking account only of adult
morphology, they have the capacity to clarify longer lengths
of various developmental trajectories which may go back to
early stages of development.
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. Asimetría y modularidad del hueso hioides. Int. J. Morphol., 32(1):251-
260, 2014.
RESUMEN: La variación morfológica es el resultado de la interacción entre múltiples factores. Para huesos hioides, las diferen-
cias de forma y tamaño han sido poco mencionadas en la literatura y se limitan a estudios del dimorfismo sexual o distribución etaria.
Hasta donde sabemos, el hueso hioides humano, a diferencia de otros huesos craneales, no ha sido utilizado para hacer frente a interrogantes
del desarrollo en términos de asimetría o de la modularidad. Utilizamos métodos basados en hitos de la morfometría geométrica y en el
enfoque estadístico multivariado para estudiar la morfología del hueso hioides humano, representado por el cuerpo del hioides y astas
mayores, en una muestra de 211 huesos fusionados y no fusionadas. Dentro de un análisis de la variación de la muestra, se demostró que
el hueso hioides es por naturaleza un hueso asimétrico, que exhibe tipos de asimetría tanto direccionales y fluctuantes, compuesto de
elementos anatómicos bien integrados para los cuales, la carga biomecánica de músculos vinculados es el factor más determinante de la
variación. Sin embargo, la covarianza y la evidencia de la cantidad desigual de asimetría fluctuante entre módulos sugiereun cierto grado
de independencia durante las primeras etapas de desarrollo.
PALABRAS CLAVE: Hueso hioides; Asimetría; Modularidad; Morfometría geométrica.
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Correspondence to:
Department of Anthropology
Faculty of Science
Masaryk University
Kotlárˇská 2, 611 37 Brno
CZECH REPUBLIC
Email: urbanova@sci.muni.cz
Received: 19-09-2013
Accepted: 19-11-2013
URBANOVÁ, P.; HEJNA, P.; ZÁTOPKOVÁ, L. & SˇAFR, M. The asymmetry and modularity of the hyoid bone. Int. J. Morphol., 32(1):251-260, 2014.
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