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: email@example.com 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. LITERATURE CITED Ahlborg HG, Johnell O, Turner CH, Rannevik G, Karlsson MK. 2003. Bone loss and bone size after menopause. N Engl J Med 349:327–334. Annett M. 1985. Left, right, hand, and brain: the right shift theory. London: LEA Publishers. Arabaolaza I, Ponce P, Boylston A. 2006. Skeletal analysis. In: Adams J, Colls K, editors. ‘‘Out of darkness, cometh light’’: life and death in 19th-century Wolverhampton. Oxford: Archaeopress. p 25–38. Auerbach BM, Ruff CB. 2006. 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