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Bilateral asymmetry of the humerus during growth and development.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:639–646 (2011)
Bilateral Asymmetry of the Humerus During Growth
and Development
Amanda Blackburn*
Department of Anthropology, University of Manitoba, Winnipeg, MB R3T 5V5, Canada
KEY WORDS
handedness; biomechanics; skeletal morphology
ABSTRACT
The
development
of
handedness
throughout growth can be investigated by using bilateral
asymmetry of the humerus as a proxy for this trait. A
large skeletal sample of nonadults from English archaeological sites was examined using standard metric techniques to assess when right-sided asymmetry first appears
in the human skeleton. Results of this work indicate a
change in directional asymmetry during growth and development, with infants and young children exhibiting
no significant asymmetry and older children and adolescents demonstrating right-sidedness. This trend is con-
sistent with what has been observed in previous studies
of upper limb asymmetry in skeletal material and behaviorally in living children, adding further strength to the
premise that biomechanical forces strongly influence
bilateral asymmetry in the upper limb bones. Variability
in the magnitude of asymmetry between different features of the humerus was also noted. This characteristic
can be explained by differing degrees of genetic canalization, with length and articular dimensions being more
strongly canalized than diaphyseal properties. Am J
Phys Anthropol 145:639–646, 2011. V 2011 Wiley-Liss, Inc.
There are few traits that can be considered uniquely
human, and among them is our preference for righthandedness. It is well-established that the majority of
humans are right-handed, that is, they use their right
hand for most one-handed tasks. Overall, 90% of individuals exhibit right-handedness while left-handedness
accounts for the remainder (Porac et al., 1980; Porac and
Coren, 1981; Raymond and Pontier, 2004). Although this
proportion may fluctuate somewhat among populations,
and according to the criteria used for measuring handedness, right-handers far outnumber left-handers (Bryden
et al., 1993; Marchant and McGrew, 1998; Faurie et al.
2005). However, the process through which handedness
develops in children remains uncertain, with many children exhibiting a preference for the left hand early in
life (Corballis, 1983). It is less certain how hand preference is reflected in the bones of nonadult individuals.
Although this asymmetry is well-documented in adult
skeletons, it is uncertain whether bones of the upper
limb display behaviorally induced asymmetry early in
development or if this only becomes apparent later in
life. This raises uncertainty about whether biomechanical or genetic factors are responsible for asymmetry.
During development the skeleton increases in size and
strength (Jee and Frost, 1992). Although much of this
morphological change results from environmental,
genetic, and hormonal factors, mechanical influences
play a significant role in development and the determination of skeletal form (Kontulainen et al., 2003). However, whether the presence of bilateral asymmetry in
utero is primarily influenced by biomechanical factors or
intrinsic genetic and hormonal stimuli remains undetermined. For example, fluctuating asymmetry, which is
directionally random departures from perfect symmetry,
occurs in paired bones because of random genetic and
environmental disturbances during morphogenesis
(Leung et al., 2000). On an individual level fluctuating
asymmetry is suggestive of developmental instabilities
that can arise independently of hand preference, a point
which must be taken into account when using bilateral
asymmetry as a proxy for hand preference. Directional
asymmetry can also result from innate factors leading to
a side bias in skeletal asymmetry. This could include a
process, such as a left-right difference in blood oxygen
level, which would potentially lead to unequal bone
growth (Steele, 2000). Pande and Singh (1971) examined
the muscles and bones from the upper limbs of 10
fetuses who did not reach full-term. Results indicated
that in 9 of the 10 individuals, total muscle and bone
weight was greater in the right limb. This is consistent
with known proportions of right- to left-handers in modern human populations (Porac et al., 1980; Porac and
Coren, 1981; Annett, 1985; Raymond and Pontier, 2004;
Blackburn and Knüsel, 2006). Schultz (1926) also found
that in fetuses the right humerus was longer than the
left in over 50% of cases (n 5 623). Bareggi et al. (1994)
conducted a study using a sample of 58 aborted embryos
and fetuses aged between 8 and 14 weeks. In almost all
cases the right humerus, radius, and ulna proved to be
longer than their left counterparts. It is unclear, however, whether the sample was naturally or medically
aborted; natural abortions could introduce error from pathological conditions which may affect asymmetry. Hepper et
C 2011
V
WILEY-LISS, INC.
C
Grant sponsors: Social Sciences and Humanities Research Council
of Canada, Faculty of Graduate Studies, University of Manitoba,
Canada Research Chairs program (RD Hoppa).
*Correspondence to: Amanda Blackburn, Department of Anthropology, 435 Fletcher Argue Building, University of Manitoba, Winnipeg, MB R3T 5V5, Canada. E-mail: umblack4@cc.umanitoba.ca
Received 6 September 2010; accepted 19 April 2011
DOI 10.1002/ajpa.21555
Published online 23 June 2011 in Wiley Online Library
(wileyonlinelibrary.com).
640
A. BLACKBURN
TABLE 1. Sample distribution
Age groups (n)
Site
Raunds Furnells,
Northamptonshire
St. John’s Priory, Box Lane,
Pontefract, W. Yorkshire
Blackfriars, Dominican Friary,
Gloucester
Hereford Cathedral Close,
Herefordshire
Hospital of Ss. James and Mary
Magdalene, Chichester
St. Peter’s Collegiate Church,
Wolverhampton
California cemetery, Baldock,
Hertfordshire
Kingsholm, Gloucester
Blackgate, Newcastle upon Tyne
St. Martin’s Church, Wharram
Percy, N. Yorkshire
Ancaster, Lincolnshire
Context
1
2
3
4
Total
Medieval; rural; agricultural (Boddington, 1996)
8
21
12
10
51
Medieval; rural; agricultural (Lee, 1989)
0
6
5
6
17
Medieval; friary and possible hospital (Wiggins
et al, 1993)
Medieval; urban (Stone and Appleton-Fox,
1996)
Medieval; almshouse (Magilton and Lee, 1989)
0
7
4
6
17
7
0
23
10
40
7
21
12
11
51
Industrial; urban (Arabaolaza et al., 2006)
9
6
2
10
27
Romano-British; small village at a crossroads
(Roberts, 1988)
Romano-British; urban (Roberts et al., 2004)
Medieval; urban and rural (Nolan, 1998)
Medieval; rural; agricultural (Mays, 2007;
Steele and Mays, 1995)
Romano-British; small defended settlement
(Mays and Faerman, 2001)
0
0
3
4
7
0
27
23
2
27
59
2
9
23
3
4
14
7
67
119
8
17
6
6
37
84
166
101
84
435
Total (n)
Age group 1 5 fetus–12 months; 2 5 1–8 years; 3 5 9–17 years; 4 5 181 years.
al. (1991) found direct evidence for mechanical influences in
the form of thumb-sucking. An ultrasound study demonstrated that 90% of fetuses had a preference for sucking
their right thumb (Hepper et al., 1991). This finding not
only suggests that right-handedness is present before birth,
but that mechanical influences may be responsible for the
skeletal asymmetry observed in the human fetus, although
this evidence is still somewhat circular as the asymmetry
could be present before the movement occurs.
Other studies have produced results indicating that
left-sidedness is present before birth or early in development (Steele and Mays, 1995). Bagnall et al. (1982)
found the left humerus to be longer in a large sample of
fetuses aged 8 to 26 weeks. Steele (2000) points out,
however, that it is best to make inferences from either
full-term fetal skeletal remains or live full-term neonates
as there is less possibility of pathological conditions
affecting results. Any interpretation based on the study
of nonsurvivors should be made cautiously as this group
may not accurately represent typical patterns of growth
and development (Wood et al., 1992).
Observation of modern children demonstrates that
hand preference tends to emerge between 18 and 24
months of age, usually in conjunction with the first use
of two-syllable words (Ramsay, 1980; Hepper et al., 1991;
Butterworth and Hopkins, 1993). Until the age of 8
years, hand preference fluctuates, with an increasing
preference for the right hand (Corballis, 1983). It could
be these fluctuations in behavioral development that are
reflected in the observed lack of clear directional asymmetry among infants and young children.
Although the development of behavioral handedness
has been observed in children (Ramsay, 1980; Butterworth and Hopkins, 1993), how it presents in the skeleton throughout growth is not well established. Previous
work with the humerus in a living population also supports the hypothesis that dimensions of this element are
reflective of both hand preference and activity (Blackburn and Knüsel, 2006). On the basis of what is understood of biomechanics and the fluctuating hand preference in young children, it is predicted that nonadult
American Journal of Physical Anthropology
skeletons will exhibit different patterns of bilateral
asymmetry than their adult counterparts, exhibited as
left-sided dominance or symmetry between the two
humeri. Furthermore, asymmetry in limb bone dimensions should only develop once repetitive bilateral activity commences, as it does after 18–24 months of age.
This study investigates whether upper limb asymmetry
is a trait present at birth or one developed throughout
life. It further examines total absolute asymmetry to
determine if there are variations in the magnitude of
this trait.
MATERIALS AND METHODS
A total of 11 archaeological skeletal populations from
England were used in this study, ranging in time from
the Romano-British period to the 19th century (Table 1).
Although the majority of individuals were nonadults
(less than 18 years of age) a small sample of adult individuals was examined for comparative purposes. Sites
containing large numbers of nonadults were favored,
and individuals included in this study were required to
have both humeri relatively well-preserved and to be
free of obvious pathological alterations. The number of
adults sampled was limited to 20% of the total nonadult sample so as not to overwhelm the main focus of
this work. The adults were chosen randomly with no
preference for age or sex.
Age categories
In all instances, age and sex data were obtained from
existing skeletal reports and analyses compiled by previous researchers (Roberts, 1988; Cox, 1989; Boulter and
Rega, 1993; Wiggins et al., 1993; Lee, 2001; Arabaolaza
et al., 2006; Boylston, personal communication; Mays,
personal communication). Sex was determined in older
adolescents and adults using pelvic and cranial traits. In
some instances sex was recorded for younger nonadults
as well, however, these data were not incorporated into
the present research because of the problems associated
641
UPPER LIMB ASYMMETRY IN NONADULTS
with reliably assigning sex in juvenile skeletal remains
(Scheuer, 2002; Vlak et al., 2008). In nonadults, ages
were based on dental development and eruption, as well
as long bone length and epiphyseal fusion. In adults, age
was based primarily on pubic symphyseal and auricular
surface changes. For cases where these features were
poorly preserved, molar attrition, appearance of sternal
rib ends, and the presence of degenerative joint disease
were used. It is acknowledged that some error may be
introduced from the use of both multiple researchers and
multiple techniques. However, given the breadth of the
age groups in the current study, these errors are likely
to be minimal. Each individual was subsequently
assigned to one of four age categories (fetus-12 months;
1–8 years; 9–17 years; 181 years). This system divides
the nonadults into groups based on previous studies of
handedness in children, which consider the behavioral
implications of each age category. These groups allow for
comparisons of age-related behavior, while maintaining
reliability in the actual ages assigned. Adults were initially divided into additional age subgroups and Kruskal-Wallis tests were performed for all measurements to
determine if there was a difference in median directional
and absolute asymmetry between these categories. In all
cases there was no significant difference between any of
the adult age groups. All subsequent analyses consider
individuals 18 years of age and older as one category.
Measurements
Three measurements were obtained from each humerus
wherever possible. Maximum length was taken to the
nearest millimeter, by means of a standard osteometric
board according to Brothwell’s (1981) definition. This measurement was taken from the medial margin of the trochlea to the end of the head. In humeri where the epiphysis
was unfused, measurement was taken from the medial
margin of the metaphysis to the proximal margin. To take
maximum length the most proximal and most distal areas
had to be intact. Sliding calipers were used to obtain the
epicondylar breadth to the nearest 0.1 mm by measuring
from the furthest protruding point on the lateral epicondyle to the equivalent point on the medial epicondyle
(Buikstra and Ubelaker, 1994). In instances where the epicondyles were not fused, the maximum distal mediolateral
metaphyseal breadth was obtained, although it is referred
to in all subsequent analyses as the epicondylar breadth.
Maximum midshaft diameter was also taken with dial calipers to the nearest 0.1 mm. Midshaft is defined as half of
the maximum length of the element with the diameter
taken by rotating the sliding calipers until the maximum
measurement is obtained. In some instances the midshaft
was estimated in elements where the total length was not
calculated due to minor cortical erosion. Midshaft was
only estimated in those instances where it could be reliably determined.
Calculation of asymmetry
In each individual asymmetry was standardized by
means of the following equation (Van Valen, 1962):
standardized asymmetry ¼
RL
3100
ðR þ LÞ=2
where R is the right measurement and L is the left measurement. The use of this directional asymmetry formula
serves to provide a measure of both the direction and
degree of asymmetry expressed in each individual case.
The absolute value of directional asymmetry was also
considered, allowing the magnitude of asymmetry to be
observed irrespective of direction. Both directional and
fluctuating asymmetry contribute to this value making it
representative of total asymmetry.
To account for any potential bias introduced through
combining samples, all data were divided according to
age group and Kruskal-Wallis tests were performed to
detect any variations in asymmetry between sites. In all
instances no significant differences were found and all
sites were considered together in further analyses. The
same procedure was followed for sex as previous studies
have reported variations between males and females
(Hrdlicka, 1932; Münter, 1936; Constandse-Westermann
and Newell, 1989; Sakaue, 1998); this variable was
assessed in 75 individuals from the adolescent and adult
sample. Of these individuals, 30 were female and 45
were male. Kruskal-Wallis tests revealed no significant
differences in asymmetry between sexes and these data
were subsequently pooled.
All measurement data were analyzed using SPSS 18.
Directional and absolute asymmetry results were tested
for a normal distribution using the Shapiro-Wilk test of
normality, which indicated a non-normal distribution for
all measurements (P \ 0.001). Therefore, all subsequent
tests were performed on median values, although mean
asymmetries are included in summary statistics to facilitate comparison with other studies. Wilcoxon one-sample
signed-ranks tests were used to determine if there was
significant directional or absolute asymmetry for each
variable within age groups. Kruskal-Wallis tests were
performed for the directional and absolute asymmetry of
each measurement to determine if there is significant
variation between the four age groups. Following Auerbach and Ruff (2006), posthoc pair-wise comparisons
between age groups for measurements found to be significant by the Kruskal-Wallis tests were made using
Mann-Whitney U-tests.
Repeatability of measurements
The repeatability of measurements was estimated
through the re-measurement of twenty-two randomly
selected nonadult humeri. It should be noted that a
small portion of these humeri were from populations separate from the research sample. This factor should not
affect results of this test as there is nothing inherent in
any of the populations that should affect measurement
repeatability. Of the re-measured humeri, 9 of the 22 elements represent individuals less than 5 years of age. As
many of the remeasured elements were unpaired, a
Technical Error of Measurement test could not be performed to assess the repeatability of asymmetry scores.
Instead, the average percent difference between repeated
measurements was compared with the average difference between right and left sides in the total nonadult
sample. Results indicate that in all cases the average difference between repeated measurements is small compared with the difference between right and left sides
(Table 2).
RESULTS
Analysis of median standardized asymmetry for each
measurement by age category shows that three measureAmerican Journal of Physical Anthropology
642
A. BLACKBURN
TABLE 2. Measurement error
Age group
Fetus–4 years
Measurement
Length
Midshaft diameter
Epicondylar breadth
5–17 years
Length
Midshaft diameter
Epicondylar breadth
Sample
N
Mean difference (%)a
Standard deviation
Total
Remeasurements
Total
Remeasurements
Total
Remeasurements
Total
Remeasurements
Total
Remeasurements
Total
Remeasurements
39
9
154
9
19
9
89
13
176
13
42
13
0.65
0.20
3.35
0.30
2.48
0.03
1.19
0.00
3.25
0.59
1.83
0.15
0.83
0.30
3.41
0.97
2.65
0.03
1.23
0.00
3.20
0.57
1.47
0.32
a
Percent difference for the total sample measures the mean difference between right and left sides compared with the total measurement (e.g., total length of humerus); percent difference for remeasurements reports the mean difference between repeat measurements as a percentage of the total measurement.
Fig. 1. Box plot of directional length asymmetry by age
group.
Fig. 3. Box plot of directional epicondylar breadth asymmetry by age group.
TABLE 3. Directional asymmetry within age groups
Age groups
Fetus–12 months
1–8 years
9–17 years
181 years
Fig. 2. Box plot of directional midshaft diameter asymmetry by age group.
ments commence as symmetrical among infants
and gradually change to right-sided during growth
(Figs. 1, 2, and 3). Wilcoxon signed-ranks tests indicate
American Journal of Physical Anthropology
Mean
N
SD
Median
P-value
Mean
N
SD
Median
P-value
Mean
N
SD
Median
P-value
Mean
N
SD
Median
P-value
Length
Midshaft
diameter
Epicondylar
breadth
20.23
33
1.09
0.00
0.140
0.43
95
0.96
0.57
\0.001
1.14
56
1.62
1.26
\0.001
1.28
59
1.13
1.27
\0.001
0.51
81
5.07
0.00
0.402
1.79
153
3.69
1.64
\0.001
1.33
97
4.87
1.44
\0.001
2.17
83
3.59
2.01
\0.001
21.54
17
3.54
20.80
0.109
0.75
19
2.09
0.32
0.068
1.12
30
2.05
1.48
0.003
0.42
50
2.34
0.88
0.113
Bold indicates asymmetry is significant at P \ 0.05 (Wilcoxon
signed-ranks test). SD is standard deviation.
643
UPPER LIMB ASYMMETRY IN NONADULTS
TABLE 4. Comparison of asymmetry (probability values) between age groups
Directional asymmetry
Absolute asymmtry
Groups
Length
Midshaft diameter
Epicondylar breadth
Length
Midshaft diameter
Epicondylar breadth
All age groupsa
Pair-wiseb
Group 1–2
Group 1–3
Group 1–4
Group 2–3
Group 2–4
Group 3–4
\0.001
0.022
0.013
\0.001
0.944
0.794
\0.001
\0.001
\0.001
\0.001
\0.001
0.367
0.017
0.026
0.004
0.914
0.298
0.359
0.018
0.002
0.031
0.378
0.658
0.103
0.319
\0.001
\0.001
\0.001
\0.001
0.739
0.581
0.708
0.901
0.896
0.688
0.762
0.579
0.929
0.795
0.286
0.397
0.889
a
P values for Kruskal–Wallis tests.
P values for Mann–Whitney U tests.
Age group 1 5 fetus–12 months; 2 5 1–8 years; 3 5 9–17 years; 4 5 181 years.
Bold indicates that asymmetry between age groups is significant at P \ 0.05.
b
that directional asymmetry is nonsignificant among
infants, but deviates significantly in the oldest three age
groups for midshaft diameter and length and in the 9- to
17-year-old age group for epicondylar breadth (Table 3).
Kruskal-Wallis tests demonstrate significant variation in
the magnitude of directional asymmetry for all measurements between age groups (Table 4). Posthoc pair-wise
tests further indicate that for all measurements there is a
significant difference between infants and all other age
groups. It should again be noted, however, that epicondylar breadth shows no significant difference between left
and right sides before 9 years of age, casting doubt on the
biological relevance of the results of the pair-wise comparison for this measurement. Length also shows an increase
between 1- and 8-year-olds and all older age groups which
is, in this instance, corroborated by significant intra-age
asymmetry (Table 4). Thus, age-related increases in directional asymmetry of humeral length show a gradual
increase throughout childhood (see Fig. 1).
The Wilcoxon signed-rank tests indicate that absolute
asymmetry deviates significantly from zero in all age
groups (Table 5). Between age-group comparisons however, demonstrate a significant difference in absolute
asymmetry only for length (Table 4; Fig. 4). Posthoc
pair-wise tests show that this difference exists between
the youngest group (fetus: 12 months), which shows very
little absolute asymmetry, and all individuals over the
age of 9 (Table 4). Thus, absolute asymmetry remains
relatively constant for diaphyseal and epicondylar
breadths, but shows an age-related increase for length,
following very low values among infants.
DISCUSSION
Median humeral directional asymmetry values among
adults in the present study are somewhat lower than but
not considerably different from those reported by Auerbach and Ruff (2006) for adult ‘‘preindustrial Europeans’’.
Median adult asymmetry in the current sample is 1.27%,
2.01%, 0.88% for length, diaphyseal diameter, and epicondylar breadth respectively. This compares to Auerbach
and Ruff ’s (2006) results of 1.95, 2.72, and 1.28% for the
same properties. This similarity supports the interpretation that the sample is ‘‘normal’’ in terms of patterning
and magnitude of asymmetry among adults. The combined measurements demonstrate increasing right-sided
asymmetry throughout growth. When examining median
directional asymmetry for each measurement by age category, a statistically significant trend was observed
between age groups. This is particularly apparent when
TABLE 5. Absolute asymmetry within age groups
Age groups
Fetus–12 months
1–8 years
9–17 years
181 years
Mean
N
SD
Median
P
Mean
N
SD
Median
P
Mean
N
SD
Median
P
Mean
N
SD
Median
P
Length
Midshaft
diameter
Epicondylar
breadth
0.67
33
0.88
0.00
0.001
0.77
95
0.704
0.68
\0.001
1.47
56
1.31
1.38
\0.001
1.42
59
.95
1.32
\0.001
3.59
81
3.60
2.89
\0.001
3.06
153
2.72
2.37
\0.001
3.27
97
3.83
2.63
\0.001
3.24
83
2.65
2.78
\0.001
2.45
17
2.95
1.84
0.001
1.57
19
1.53
1.51
\0.001
1.83
30
1.42
1.78
\0.001
1.83
50
1.48
1.46
\0.001
Bold indicates asymmetry is significant at P \ 0.05 (Wilcoxon
signed-ranks test). SD is standard deviation.
comparing the youngest age group to the remainder of the
sample. The sampled skeletal populations demonstrate
symmetry until approximately 12 months of age. There
was a slight tendency for left-sidedness in the epicondylar
breadth of young infants, but it did not reach statistical
significance. Studies of individuals of similar age to the
current work support the observation that asymmetry
becomes increasingly right-sided during growth (Van
Dusen, 1939; Ingelmark, 1946; Steele and Mays, 1995).
Although some previous research has found right-sided
asymmetry early in development, much of that work is
based on prenatal samples (Schultz, 1926; Pande and
Singh, 1971; Bareggi et al., 1994). This could suggest that
shifts in asymmetry occur between embryonic development, birth, and the first several months of life. The finding of symmetry at birth in the studied populations does
not support the hypothesis that right-sided asymmetry of
the humerus is present at birth or shortly thereafter.
The results obtained here are consistent with what is
known about the development of behavioral handedness
exhibited in young children. Children usually begin to
demonstrate hand preference between 1.5 and 2 years of
age. This coincides with the development of spoken lanAmerican Journal of Physical Anthropology
644
A. BLACKBURN
Fig. 4. Box plot of absolute length asymmetry by age
group.
guage, which suggests a correlation (Ramsay, 1980; Butterworth and Hopkins, 1993). The results of this study
demonstrate a change from symmetry to right-sidedness
early in development, after 1 year of age. At birth and
shortly thereafter, both directional and absolute diaphyseal breadth asymmetry is variable across sides. This is
similar to what is observed behaviorally and, from a biomechanical perspective, what would be expected if there
was no hand preference or if that preference continually
shifted back and forth during infancy. These results are
also consistent with the locomotor behavior of infants
and young children. Crawling commences during the
first year of life and gradually shifts to walking at 12
months of age. Because crawling necessitates the relatively equal use of both arms, upper limb symmetry
would be expected during this stage of life. After walking
begins and consistent hand preference develops, mechanical directional factors become significant. Diaphyseal
dimensions respond rapidly to this mechanical change,
whereas length and epicondylar breadth gradually develop adult levels of asymmetry several years afterwards. This is similar to what Ruff (2003) observed in
the Denver Growth Sample where rapid changes in femoral/humeral diaphyseal strength occurred shortly after
walking commenced. Conversely, length proportions did
not change with the initiation of walking (Ruff, 2003).
Therefore, changes in asymmetry throughout growth
suggest that while this trait may be based to some
extent on biomechanical modifications, the relationship
between mechanical stimuli and asymmetry is not
straightforward.
Observation of different measurements indicates that
magnitude of absolute asymmetry varies according to
anatomical feature. In the total sample (pooled across
ages) diameter of the diaphyseal midshaft exhibits the
most asymmetry, followed by epicondylar breadth and
length, respectively. This is similar to Auerbach and
Ruff ’s (2006) observation that diaphyseal asymmetry
exceeded that of length and articular surfaces in a sample of 780 adult individuals. These results can be attributed to several factors, including the ability of the diaphysis to continue remodeling in response to activity
once physical maturity has been reached whereas length
and articular dimensions remain relatively static (Garn
American Journal of Physical Anthropology
et al., 1967; Lazenby, 1990; Ruff et al., 1991; Heaney et
al., 1997; Humphrey, 1998; Lieberman et al., 2001; Ahlborg et al., 2003). It also points to the humerus as being
modular, in that it can be subdivided into discrete, yet
connected, areas (Hallgrı́msson et al., 2002; Klingenberg,
2008). Auerbach and Ruff (2006) hypothesize that the
difference in magnitude of asymmetry between humeral
dimensions could result from some areas being more sensitive to perturbations during growth. This could indeed
account for the variations witnessed in the current work.
These patterns may be attributable to varying degrees of
genetic canalization, with length being the most canalized throughout growth and, therefore, the least susceptible to biomechanical influences. Conversely, diaphyseal
breadth is the least genetically canalized and, consequently, most responsive to mechanical stimuli. Epicondylar breadth can be placed somewhere between length
and diaphyseal dimensions in terms of canalization; the
distal end of the humerus does not appear to be as
strongly constrained by genetic influences as length, but
it does not respond as vigorously to movement and mechanical strain as the diaphysis. These conclusions are
consistent with Auerbach and Ruff (2006) who hypothesized decreasing developmental canalization from
lengths to articular breadths to diaphyseal breadths.
Finally, the possibility that this sample of nonadults
may not represent the average population needs to be
acknowledged. Wood et al. (1992) argue that data from
osteological analyses are biased. This is particularly relevant for studies of nonadults as they represent the individuals who did not survive to adulthood. However,
Lovejoy et al. (1990) propose that infant and child death
likely results from acute infection, rather than a chronic
disease process. Therefore, these individuals likely do
represent the same pattern of population growth and,
hence, upper limb asymmetry, as was experienced by
those who did survive. Selective mortality, then, should
not be a confounding factor. There was also some concern regarding the appropriateness of combining samples from a wide range of archaeological populations as
lifestyle would have changed throughout time. However,
statistical tests indicated no difference in asymmetry
between samples. This is somewhat surprising given
that differences in asymmetry have been noted between
populations, and even subsamples of populations, based
on factors such as economy and class (Constandse-Westermann and Newell, 1989; Auerbach and Ruff, 2006).
However, many of the population samples here were relatively small (within age groups), which may have contributed to the lack of significant differences found
among them. Further research could be conducted using
several populations from different geographical locations.
Ideally a portion of these groups should have activity
patterns and lifestyles that are similar to the English
populations included in the current study. In this manner, it may be possible to elucidate patterns in the
development of asymmetry based on biomechanical and
genetic influences.
CONCLUSIONS
Upper limb bilateral asymmetry is ubiquitous among
modern adult humans. Previous studies however, have
produced conflicting results regarding how asymmetry
develops during growth. This research focused on a large
sample of English archaeological skeletons, dating from
the Romano-British period to the 19th century. The non-
UPPER LIMB ASYMMETRY IN NONADULTS
adult portion of the sample was divided into three age
groups that broadly distinguish between infants, young
children, and adolescents. Measurements were obtained
for the total length, midshaft diameter, and epicondylar
breadth of paired humeri. Results demonstrate that
among infants, absolute asymmetry is very low for
length but is larger and equivalent to that for older
children/adolescents for diaphyseal and epicondylar
breadths. Directional asymmetry is not present in
infants for any dimension. After one year of age however, directional asymmetry appears to be fully developed in the diaphysis, but is more subtle in epicondylar
breadth and length. In these latter dimensions, directional asymmetry develops more gradually throughout
childhood, only reaching adult values in the 9–17 year
age group. The variability in asymmetry between these
discrete areas of the humerus can be explained by differing degrees of genetic canalization, with length and
articular dimensions being more strongly canalized than
diaphyseal properties. Before the development of handedness, this is manifested as more absolute (random)
asymmetry in diaphyseal and epicondylar breadths than
in length, and after the development of handedness, in
the more rapid increase in directional asymmetry in diaphyseal breadth. These results support the hypothesis
that there is an inverse relationship between the degree
of canalization and the influence of mechanical stimuli
on skeletal dimensions and asymmetry.
ACKNOWLEDGMENTS
The author would like to gratefully acknowledge Drs.
Robert Hoppa, Mary Silcox, Richard Lazenby, Stacie Burke
and Martin Reed for providing valuable feedback during all
stages of this project. The comments of Dr. Christopher
Ruff, one Associate Editor, and two anonymous reviewers
are also greatly appreciated. This research required the assistance of many individuals in order to access various
archaeological collections and skeletal reports: Dr. Jo Buckberry and Mrs. Anthea Boylston (University of Bradford);
Dr. Pia Nystrom and Dr. Andrew Chamberlain (University
of Sheffield); Dr. Simon Mays (English Heritage); Pamela
Mayne Correia, Nicole Burt, and Megan Caldwell (University of Alberta). Without your help and cooperation this
work would not have been possible.
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