Patterns of Directional Asymmetry in the Pelvis and Pelvic Canal

AMERICAN JOURNAL OF HUMAN BIOLOGY 00:00–00 (2016)

Original Research Article Patterns of Directional Asymmetry in the Pelvis and Pelvic Canal

1,2 3 1 VICTORIA A. TOBOLSKY, * HELEN K. KURKI, AND AND JAY T. STOCK 1Division of Biological Anthropology, Department of Archaeology and Anthropology, University of Cambridge, Cambridge, UK 2Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 3Department of Anthropology, University of Victoria, Victoria, British Columbia, Canada V8W 3P5

Objectives: The human pelvis is unique among modern taxa for supporting both parturition of large brained young and obligate bipedalism. Though much work has focused on pelvic development and variation, little work has explored the presence or absence of asymmetry in the pelvis despite well-known patterns of asymmetry in other skeletal regions. This study investigated whether patterns of directional asymmetry (DA) could be observed in the pelvis or pelvic canal. Methods: Seventeen bilaterally paired osteometric measurements of the os coxae (34 measures in total) were taken from 128 skeletons (female n 5 65, male n 5 63) from recent human populations in five geographic regions. Paired sample t-tests and Mann–Whitney U-tests were used to investigate DA. Results: Results from a pooled sample of all individuals showed that the pelvis exhibited a left-bias in DA. In contrast, the pelvic canal exhibited a pattern in which the anterior canal exhibited a right-bias and the posterior canal exhibited a left-bias. Neither sex nor populational differences in DA were observed in the pelvis or pelvic canal. Conclusions: The varying patterns of asymmetry uncovered here accord with prior work and may indicate that loading from the trunk and legs place differing stresses on the pelvis and canal, yielding these unequal asymmetries. However, this is speculative and the possible influence of genetics, biomechanics, and nutritional status on the development of pelvic and canal asymmetries presents a rich area for future study. Additionally, the potential influence of pelvic canal asymmetry on obstetric measures of pelvic capacity merits future research. Am. J. Hum. Biol. 00:000–000, 2016. VC 2016 Wiley Periodicals, Inc.

The architecture of the modern human pelvis has long 2006), while others have noted populational differences in been argued to be adapted to the competing requirements variance in the pelvis, canal, and long bones (Kurki and of bipedalism and birth (Krogman, 1951; Washburn et al., Decrausaz, 2016), some of which may be genetic in origin. 1960; but see Rosenberg and Trevathan, 1995, 2002; Wells The influence of ontogenetic insults may also contribute et al., 2012; Dunsworth et al., 2012; Grabowski et al., to the development of the skeleton and associated asym- 2011; Grabowski and Roseman, 2015). As a result, the pel- metries (e.g., Beasley et al., 2013; Palmer and Strobeck, vis is characterized by a mosaic pattern in morphology 1986; but see Tomkinson and Olds, 2000), though the rela- and development not observed in any known primate tive influence of developmental instability, particularly taxa, extant or extinct (DeSilva, 2011; Kibii et al., 2011; nutritional deficiencies, on pelvic development is poorly Leutenegger, 1974; Lovejoy et al., 2009; Rak and Are- delineated. Some suggest a disproportionate effect on nsburg, 1987; Rosenberg, 1988; Schultz, 1930, 1949); pubic bone morphology (e.g., Greulich and Thoms, 1938; these unusual traits also yield a long and difficult labor in Kelley and Angel, 1987; Nicholson, 1945; see Wells et al., human mothers, the unique rotational mechanisms and 2012 for discussion), but this relationship is putative and associated mortality of which are well-documented in remains to be rigorously tested. Biomechanical loading is both modern and archaeological populations (e.g., Angel, also known to heavily influence the development of direc- 1946; Baltag, 2009; Derry, 1935; Rosenberg and Treva- tional asymmetries in long bones and tends to more heav- than, 2002; Wells, 1975; WHO, 2005, 2012). ily influence bone diaphyses than epiphyses to preserve Recent studies have increasingly emphasized factors the integrity of joint motion (Lieberman et al., 2001, 2003, influencing the relative plasticity of pelvic shape and 2004; Stock, 2006; but see Plochocki, 2004), though to obstetric capacity (e.g., Kurki, 2007, 2011a,b, 2013a,b; what extent this pattern of epiphyseal canalization may Ruff, 2010), with well-documented sex differences (Abitbol, be mirrored in the pelvis is unknown. 1987; Rosenberg and Trevathan, 2002; Tague, 1991, 1992, Humans usually exhibit an upper-limb right bias, and a 2000) and population differences (Kurki, 2007, 2011b), weaker lower limb left bias (Auerbach and Ruff, 2004, some of which may be due to neutral variation (Betti et al., 2006). This pattern, referred to as crossed or contralateral 2012, 2013). However, while it is known that modern humans display a high degree of long bone bilateral asymmetry with consistent directional patterns across sexes Contract grant sponsor: Gates Cambridge Trust; Contract grant spon- and populations (Auerbach and Ruff, 2004, 2006; Hall- sor: the Fitzwilliam College Travel Fund. grimsson et al., 2002, 2003), little research has investi- *Correspondence to: Victoria A. Tobolsky, Department of Human Evolu- gated the extent to which similar patterns of asymmetry tionary Biology, Harvard University, 11 Divinity Avenue, Cambridge, MA 02138, USA. E-mail: [email protected] may be present in the pelvis (e.g., Boulay et al., 2006) or Received 1 January 2015; Revision received 18 March 2016; Accepted 1 pelvic canal. May 2016 Skeletal asymmetries arise from a number of causes, Additional Supporting Information may be found in the online version including genetic, developmental, and biomechanical of this article. influences. Prior research has illustrated regional differ- DOI: 10.1002/ajhb.22870 Published online 00 Month 2016 in Wiley Online Library ences in long bone asymmetries (e.g., Auerbach and Ruff, (wileyonlinelibrary.com).

VC 2016 Wiley Periodicals, Inc. 2 V.A. TOBOLSKY ET AL.

TABLE 1. Geographic samples and populations TABLE 2. Osteometric measurements of the pelvis

Geographic sample Population Male Female Total Measurement Description

Indo-Asia 7916Innominate length From most superior point on iliac Andaman Islands 7 9 16 (INLG) crest to most inferior point of North Africa 18 14 32 ischial tuberosity.a (Fig. 1, A) Egypt 3 1 4 Iliac height Distance from Schultz’s (1930) Point Jebel Moya 2 0 2 (ILHT) A to most superior point on iliac Nubia 10 9 19 crest.b (B) Sudan 5 3 8 Iliac breadth Distance between anterior superior Australia 6410(ILBR) and posterior superior iliac Aboriginal Australia 6 4 10 spines.b (C) North Europe 13 11 24 Pubic bone length (PBLG) Distance from point A to superior Maiden Castle (Britain) 9 7 16 aspect of symphyseal face.b (D) British War Cemetery 4 4 8 Ischium length (ISLG) Distance from point A to the mid- North America 19 27 46 point of the transverse ridge of Ketchipauan (New Mexico) 4 18 22 ischial tuberosity.b (E) Chumash (California) 15 9 24 Acetabular height (OCAH) Maximum diameter across the ace- Total Sample 63 65 128 tabulum from superoventral to post- erodorsal.b (F) Acetabulosciatic breadth Minimum distance from the poste- (OCAScB) rior border of the acetabulum to the infero-anterior margin of the asymmetry, is consistently observed across human popu- greater sciatic notch.b (G) lations (Auerbach and Ruff, 2004, 2006; Blackburn, 2011; Symphyseal height Maximum superoinferior breadth of Blackburn and Knusel, 2006; Latimer and Lowrance, (OCSH) the symphyseal surface.b (H) 1965; Steele and Mays, 1995). aMeasurement obtained using a portable Paleo-tech concepts osteometric board. Some clinical evidence suggests that the pelvis of living bMeasurement obtained using a standard Mitutoyo digital caliper. humans may manifest a left bias as a result of biomechanical co-dependence with the lower limbs (e.g., Al-Eisa et al., 2006; Badii et al., 2003; Levangie, 1999), in accord with reports of a left bias in the sacrum (Plochocki, 2002; MATERIALS AND METHODS Tague, 2007). Indeed, the sacrum is known to alter sub- stantially in shape and angulation throughout the life This study analyzed pelvic morphology of 10 recent course as a response to gait acquisition (e.g, Tardieu et al., human populations from five broad geographic regions 2013). One osteometric analysis of the os coxae suggest (n 5 128; Table 1) from which 17 bilaterally paired meas- that the pelvis exhibits a “spiral pattern” of asymmetry, ures of the pelvis and canal (34 variables total; Tables 2 according with right torsion from the weight of the trunk and 3) were collected and analyzed. and left torsion from the influence of the lower limbs in a All osteometric measurements were taken to the near- sample of 12 older adults (Boulay et al., 2006). The extent est millimeter. Tools used included a Mitutoyo standard to which these patterns are replicable, whether these or gage caliper (recorded at 0.01 mm precision), a Paleo- other patterns are observed within the pelvic canal, and tech concepts portable osteometric board, and a standard how such patterns might differ by population or sex is measuring tape. All measurements have been previously unknown. defined and used in the literature (e.g., Kurki, 2007, Due to the known correlations between asymmetry 2011a,b; Rosenberg et al., 1988; Tague, 1989, 1991, 1992, and mechanical loading in other parts of the body, 2000) with the exceptions of SAS1L and SAX, which asymmetry in the pelvis is rendered of particular inter- were defined for this study (Table 2). These measures est. Given the tight constraints mechanical and obstet- were designed to calculate asymmetry in the length of ric functionality impose on the pelvis, asymmetry the costal process of the first sacral vertebra, a trait should either not be present or should be present in known to exhibit a female-biased sexual dimorphism patterns that do not compromise either function. To that increases the dimensions of the pelvic inlet (Tague, explore the incidence and patterns of asymmetry in the 2007). pelvis and pelvic canal, five sample populations from a Osteometric measures of the pelvic canal were obtained variety of geographic regions and climates were exam- from articulated pelves when afforded by skeletal preser- ined in this study, following known population differen- vation, with the exception of pelvic canal depth. Pelves ces in both pelvic size and shape (e.g., Betti et al., were articulated by securing the innominate bones and 2012, 2013; Kurki and Decrausaz, 2016; Ruff, 2010) and sacrum in anatomical position with rubber bands to in asymmetry across populations (e.g., Auerbach and ensure that no movement occurred while measurements Ruff, 2006). We test directional asymmetry (DA) as an were being taken. Following Kurki (2007, 2011a,b), no exploratory method to quantify the presence or absence adjustments were made to account for the soft tissues of of the asymmetry and its direction in the pelvis. How- the pubic symphysis and sacroiliac joints. ever, notably, this study did not attempt to elucidate Preservation varied between individuals and sample the developmental, genetic, or biomechanical mecha- populations, as is typical in skeletal analysis; this phe- nisms by which such differentiation may have occurred. nomenon often poses a particular impediment in the anal- This study investigated the pattern and magnitude of ysis of the pelvis or other fragile bones. This resulted in a pelvic asymmetry and whether these patterns differed variety of sample sizes utilized in analysis (i.e., not all by populational affilitation or sex, based on known dif- measures were collected from all 128 individuals). Simi- ferences in pelvic size and shape between populations larly, population sample sizes were frequently small and sexes. (n 5 9–46). Equal statistical power between analyses is

American Journal of Human Biology PELVIC AND CANAL ASYMMETRY 3 therefore not observed in this study, as is typical of many asymmetry (Auerbach and Ruff, 2006; Auerbach and osteometric studies. Raxter, 2008; Blackburn and Knusel, 2006; Mays, 2002; Sex determinations for this sample were undertaken Mays et al., 1999; Steele and Mays, 1995): with commonly used nonmetric pelvic variables, including ÀÁÀÁ greater sciatic notch angle, sub-pubic angle, and presence %DA 5 right2left = average of left and right 3 100 of a ventral arc (Buikstra and Ubelaker, 1994; Kurki, 2007; Mays and Cox, 2000; Phenice, 1969). Juveniles, as determined by incomplete epiphyseal fusion, and individ- DA was calculated as a percentage for each of the 17 bilat- uals with skeletal pathologies (including healed fractures) erally paired measures (Tables 1 and 2) to allow compari- were excluded from this sample. sons between individuals and measurements without the Osteometric measurements were collected by both VT interference of allometry. The ischio-pubic index was also and HK. Interobserver and intraobserver error rates were calculated following its known obstetric importance both calculated and neither was found to be in excess of (Schultz, 1949; Washburn, 1948). Measurements that 3% for any measurement reported in analyses (see supple- exhibit left directionality are represented by negative val- mentary materials for a more comprehensive discussion; ues, whereas those that exhibit right directionality are Tables S1 and S2). positive (Table 4). Calculations of asymmetry and pelvic capacity Statistical analyses DA was calculated to determine the laterality of these All statistical analyses were undertaken using IBM measurements and their relationship with contralateral SPSS version 21.0. Descriptive statistics, paired sample t- tests, and Mann–Whitney U-tests were used. TABLE 3. Osteometric measurements of the pelvic canal In all analyses, P < 0.05 (two-tailed) was considered significant. Student’s paired sample t-tests were used to Measurement Description examine significant differences between the left and right sides of a trait; hereafter referred to as significant bilat- Auricular surface length of the Maximum distance from the most sacrum (SAS1L) lateral extent of the first sacral eral asymmetry (Krishan et al., 2010; Plochocki, 2004). vertebra (S1) to the nearest lateral Mann–Whitney U-tests were used to examine sex or popu- extent of the superior auricular lation differences in DA measurements, controlling for a surface. (I) small sample size and continuous distribution of data Auricular surface length Distance from the apex of the sacrum of the sacrum to the nearest extent of the first (Correia et al., 2005; Kurki, 2007, 2011a, 2011b; Tague, from the apex (SAX) sacral vertebra.a (J) 1994, 2000, 2007, 2011). All analyses pertaining to sex dif- Inlet posterior (INPT) Curved length of linea terminalis ferences were derived from pooled population samples. from INML to apex of auricular surface.c (K) Inlet anterior (INAT) Curved length of linea terminalis RESULTS from INML to dorsomedial superior pubis.b (L) The results of analyses relating to patterns of asymme- Midplane posterior (MDPT) Apex of fifth sacral vertebra to try demonstrate several distinct patterns. In a pooled ischial tuberosity.b (M) sample of all individuals, all measures of non-canal pelvic Midplane anterior (MDAT) Ischial spine to dorsomedial inferior DA (excepting ILBR) exhibited a left-bias, consistent with pubis.b (N) Outlet posterior (OTPT) Apex of S5 to medial margin of the the left laterality of the lower limbs (Table 4). However, transverse ridge of the ischial the pelvic canal exhibited a different, mosaic pattern in tuberosity.b (O) which all measures of the posterior pelvic canal exhibited Outlet anterior (OTAT) Length of ischiopubic ramus from a left-bias, whereas all measures of the anterior pelvic ischial tuberosity to dorsomedial inferior pubis.b (P) canal exhibited a right-bias (Table 4). Significant differen- Pelvic canal depth (DPPL) Apex of auricular surface to medial ces between the left and right sides (bilateral asymmetry) aspect of the tranverse ridge of the a were found in seven of 17 bilaterally paired variables ischial tubersosity. (Q) using paired sample t-tests (Table 5). However, only one of aMeasurement obtained using a portable Paleo-tech concepts osteometric board. these seven variables (SAS1L) exhibited significant bilat- bMeasurement obtained using a standard Mitutoyo digital caliper. c eral asymmetry in both sexes, with a significant left bias Measurement obtained using a measuring tape. for both sexes (P < 0.01) uncovered using a t-test. Notably,

TABLE 4. Mean directional asymmetry in pelvic and canal measurements

Pelvic measure Mean DA 6 SD Mean DA 6 SD

Male Female Pooled Male Female Pooled

INLG 20.30 6 1.32 20.26 6 2.02 20.28 6 1.68 INPT 21.78 6 14.54 24.48 615.80 23.13 615.16 ILHT 20.51 6 2.28 0.13 6 3.80 20.19 6 3.12 INAT 1.38 6 2.75 0.86 6 4.46 1.18 6 3.50 ILBR 0.33 6 2.00 0.18 6 2.46 0.26 6 2.22 MDPT 21.03 6 5.71 1.48 6 7.10 20.01 6 6.28 PBLG 22.46 6 3.58 20.03 6 5.05 21.30 6 4.47 MDAT 0.78 6 2.87 0.77 6 2.82 0.77 6 2.79 ISLG 20.80 6 3.36 21.28 6 2.56 21.03 6 2.22 OTPT 20.54 6 6.29 20.27 6 6.70 20.43 6 6.40 OCAH 23.04 6 28.58 0.88 6 3.60 21.14 6 0.77 OTAT 0.25 6 2.94 20.13 6 3.99 0.09 6 3.40 OCAScB 20.14 6 4.16 0.49 6 3.94 20.31 6 4.14 DPPL 0.12 6 3.65 21.12 6 4.40 20.45 6 4.04 OCSH 0.02 6 7.69 210.02 6 39.68 24.40 6 27.14 SAS1L 25.25 6 7.89 23.68 6 8.78 24.45 6 8.35 IPI 21.55 6 5.21 20.24 6 3.15 20.94 6 4.38 SAX 0.48 6 8.90 0.28 6 9.60 0.38 6 9.21

American Journal of Human Biology 4 V.A. TOBOLSKY ET AL.

TABLE 5. Significant bilateral asymmetry in males and females rum, buttressing the validity of the results reported here (Boulay et al., 2006). The sacrum is also highly sensitive Males Females to biomechanical influences (Tardieu et al., 2013). It is Pelvic Pelvic also worth noting that the deviations from symmetry in measure R/L Bias P measure R/L Bias P sacral alae length may occur either by asymmetrical alae lengthening, presumably resulting from loading, or from PBLG L 0.003 ISLG L 0.028 lateral displacements of the body of the first sacral verte- SAS1L L < 0.001 OTAT L 0.028 INAT L 0.022 SAS1L L 0.006 bra, a distinction not tested in this study. Symphyseal OCAH R 0.004 height in females was found to be among the most variable dimensions of this study, and was the only measure to exhibit a sample difference of any kind, contrasting males exhibited more significant bilateral differences with evidence for epiphyseal canalization from the long than females (Table 5). bones of the appendicular skeleton (e.g., Lieberman et al., No significant differences between the sexes were 2001, 2003, 2004). However, given known alterations in observed in any DA measure in the pelvis or pelvic canal; pubic symphyseal and pubic bone morphology in response however, significant bilateral differences in pubic bone to parity and aging (e.g., Schutz et al., 2009; Tague, 1988), length are observed in males only, indicating a higher this variance is perhaps unsurprising. level of asymmetry in males (Figs. S1 and S2). Similarly, The pelvic canal exhibited a high degree of asymmetry, no significant differences were found between populations consistent with prior reports of a high degree of canal var- when sexes were pooled, and only one significant differ- iation (Kurki, 2013b); however, this asymmetry appears ence between populations were found in sex-specific anal- to be relatively uniform, and exhibits no significant differ- yses: symphyseal height differed significantly between ences in sex or sample in DA, though the absence of signif- populations in females (P < 0.009). icance could be due to small sample sizes as sex-specific means differ. In the pooled sample, all three measures of DISCUSSION the anterior canal (inlet, midplane, and outlet) exhibit a systematic right-bias. All three measures of the posterior The aim of this study was to investigate the patterns canal (inlet, midplane, and outlet) exhibit a systematic and magnitude of asymmetry both within the pelvis and left-bias. Furthermore, SAX, auricular surface length the pelvic canal, and the potential effects of sex and geo- measured to the apex of the sacrum (anteriorly placed), graphic sample on these patterns. However, few sex and exhibited a right-bias in both males and females sample differences were uncovered in this study and a (DA 5 0.378 6 9.210). This is in contrast to the left-bias of pooled sample of all individuals is discussed here in order the posteriorly placed SAS1L (DA 524.447 6 8.347), and to increase robusticity of the statistical tests. In this potentially in accord with the directional patterns exhib- study, non-canal pelvic asymmetry was found to exhibit a ited in the pelvic canal. left-bias. Asymmetry of the bony pelvis has been clinically Clear trends of directionality may be indicative of func- examined, typically in reference to lower back pain (e.g., tional loading differences within the pelvic canal. The sac- Al-Eisa et al., 2006; Badii et al., 2003; Levangie, 1999), rum serves as the pivot point for the upper body, and has scoliosis (e.g., Timgren and Soinila, 2006; Walker and been suggested to dynamically respond to the right-bias of Dickson, 1984), and cerebral palsy (e.g., Abel et al., 1999; the upper limbs with a left-directional bias (Plochocki, de Morais Filho et al., 2009). These asymmetries, how- 2002; Tague, 2007). Following the biomechanical require- ever, are often related to rotation or tilt of the pelvis due ments of the pelvis in supporting the trunk in the orthog- to ligamentous means rather than osteological asymmetry rade posture necessitated by bipedal locomotion (Husson (Al-Eisa et al., 2006; Anderson, 1984); however, a larger et al., 2010; Lazennec et al., 2013), the left-bias in the pos- left hemi-pelvis has been reported in one study (Badii terior pelvic canal may be similarly related to biomechani- et al., 2003), whereas another reports a “spiral pattern” of cal function. This hypothesis gains credence in asymmetry in the os coxae (Boulay et al., 2006). Asymme- considering that the midplane and outlet posterior meas- try in the bones of the pelvis, and the pelvic canal in par- ures are both taken from the S4-S5 fusion line. Further- ticular, has previously remained largely unknown. more, the pelvis exhibits an anterior tilt in life that serves The left-bias in the false pelvis uncovered in this study to disperse body weight posteriorly onto the sacrum (Abit- may correspond with the biomechanical requirements of bol, 1988; Barber, 2005; Tardieu et al., 2013). Conversely, the lumbar-pelvic-femoral complex that transmits the most adult humans are right-footed (Auerbach and Ruff, weight of the trunk to the lower limbs during locomotion 2006; Steele and Mays, 1995). Thus, the posterior pelvic (Husson et al., 2010; Lazennec et al., 2013; Tardieu et al., canal might be drawn to the left as a result of the torsion 2013). Previous studies report a systematic left-bias in the of the upper body, as is reported for the sacrum (Plochocki, sacrum (Plochocki, 2002; Tague, 2007), which is corrobo- 2002). The anterior pelvic canal might instead be drawn rated by this study’s finding that SAS1L (the auricular to the right due to its proximity to the right acetabulum surface length of the first sacral vertebra) exhibited the and femoral head, consistent with a right preference in greatest left-bias of any pelvic measure (mean footed tasks. DA 524.45), and the only variable to exhibit significant This analysis, however, is speculative; this study did bilateral asymmetry in both males and females. Sacral not directly test the influence of biomechanics on the measures also exhibited extremely high standard devia- development of asymmetry and the mechanisms guiding tions (SAS1L SD 5 8.35), potentially indicating a high the development of this asymmetry are unknown. Multi- level of sensitivity to biomechanical influence in this mea- ple populations representing five different geographic sure, or error. However, prior studies have found a high regions were analyzed to investigate potential genetic dif- degree of variance in asymmetry in the pelvis and sac- ferences by region, following known differences in pelvic

American Journal of Human Biology PELVIC AND CANAL ASYMMETRY 5

Fig. 1. Seventeen bilaterally paired osteometric measures were collected from the ox coxae for this study (Tables 2 and 3).

size and shape by population, some of which may be due osteometric data collection may introduce error. We dis- to neutral variation (Betti et al., 2012, 2013). Populational cussed DA measures that fall under this threshold for two stability of these patterns may further implicate the influ- primary reasons: one, osteological asymmetry in the pel- ence of biomechanics, though this has yet to be tested vic canal has remained largely unexplored, and two, devi- directly. At minimum, the tolerance of consistent patterns of ations from symmetry followed very discrete and asymmetry in these measures suggests that asymmetry unexpected patterns. Though intraobserver and interob- does not impede biomechanical function; asymmetry is not server error rates were calculated for this study (Tables well tolerated in other bodily measures in which asymmetry S1 and S2), we cannot exclude the possibility that would interfere with function (e.g., epiphyses; Lieberman observer error biased our results. Future work is needed et al., 2001, 2003, 2004; Stock, 2006; but see Plochocki, to replicate these findings in a larger sample, and subse- 2004). Similarly, this may suggest that asymmetry does not quently to elucidate the mechanisms by which this asym- impede obstetric function, but this also presents a fruitful metry arises, regarding both the patterns and direction of area for future study and was not addressed here. Within growth and considerations for the potential modularity of the canal, the opposing directional asymmetries of the ante- the human pelvis (Lewton, 2012). rior and posterior pelvis also, in effect, yield a small rotation of the pelvic canal. It is worth exploring further how this CONCLUSIONS rotation may affect obstetric capacity in females. The stability of these patterns across sexes and populations offers cre- Earlier studies have shown that pelvic morphology dence to the supposition that the net effect of these exhibits both male and female biased sexual dimorphism, asymmetries is neutral, impeding neither obstetrics or bio- sex differences in development, and differing variance mechanics, but this bears much further testing with quanti- (Correia et al., 2005; Kurki, 2007, 2011a,b, 2013a,b; LaV- tative evolutionary models. elle, 1995; Rosenberg et al., 1988; Tague, 1992, 1995, It is worth reiterating that sample sizes for analyses of 2007, 2009, 2011a,b). This study confirms that asymmetry the pelvis and canal are small. The discussed patterns of in pelvic measures similarly exhibit a high degree of var- asymmetry are observed in mean values from the pooled iance between measures and sexual dimorphism. The sample, but large standard deviations are also observed. false pelvis exhibited a consistent left-bias while the pel- Auerbach and Ruff (2006) recommend considering DA vic canal exhibited an unpredicted mosaic pattern of only when DA exceeds 0.5, noting that even meticulous directionality, with an anterior right-bias and posterior

American Journal of Human Biology 6 V.A. TOBOLSKY ET AL. left-bias. The mechanisms governing the development of Betti L, von Cramon-Taubadel N, Manica A, Lycett SJ. 2013. Global geo- this asymmetry are obscured at present. metric morphometric analyses of the human pelvis reveal substantial neutral population history effects, even across sexes. PLoS One 8(2): Many studies of hominin pelves reconstruct the pelvis e55909. by mirror-imaging portions as a result of missing fossil Boulay C, Tarideu C, et al. 2006. Three-dimensional study of pelvic asym- evidence (e.g., Kibii et al., 2011; Lovejoy et al., 2009; metry on anatomical specimens and its clinical perspectives. J Anat Weaver and Hublin, 2009). Such reconstructions should 208(1):21–33. Buikstra JE, Ubelaker DH. 1994. Standards for data collection from make note of potentially high degrees of asymmetry human skeletal remains. Fayetteville, AR: Arkansas Archaeological between the two hemi-pelves that may alter the shape Survey. and size of the pelvis, perhaps corresponding with altera- Coleman WH. 1969. Sex differences in the growth of the human bony pel- tions in the mechanisms and ease of parturition, as well vis. Am J Phys Anthropol 31(2):125–151. Correia H, Balseiro S, De Areia M. 2005. Sexual dimorphism in the human as locomotor function; this relationship requires further pelvis: testing a new hypothesis. HOMO 56(2):153–160. exploration both in modern humans and fossil hominins. de Morais Filho MC, Kawamura CM, Andrade PH, dos Santos MB, Pickel Future research should also consider the effects of biome- MR, Neto RB. 2009. Factors associated with pelvic asymmetry in trans- chanics in the development of pelvic asymmetry, as well verse plane during gait in patients with cerebral palsy. J Ped Orthopaed B 18(6): 320–324. as the possible links between aspects of skeletal and pel- Derry D. 1935. Note on five pelves of women of the eleventh dynasty in vic asymmetry to further explore a proposed lack of inte- Egypt. BJOG 42(3):490–495. gration between the pelvis and other skeletal characters DeSilva JM. 2011. A shift toward birthing relatively large infants early in (Grabowski et al., 2011; but see Lewton, 2012). Addition- human evolution. Proc Natl Acad Sci U S A 108(3):1022–1027. Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H. 2012. ally, future study that identifies patterns of asymmetry in Metabolic hypothesis for human altriciality. Proc Natl Acad Sci U S A the pelvis and pelvic canal might consider examining the 109(38):15212–15216. relationships between asymmetry and obstetric function. Grabowski MW, Polk JD, Roseman CC. 2011. Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism. Evolution 65(5):1336–1356. ACKNOWLEDGMENTS Grabowski M, Roseman CC. 2015. Complex and changing patterns of natural selection explain the evolution of the human hip. J Hum Evol 85: Many thanks are sent to curators Robert Kruszynski 94–110. (Natural History Museum, London) and Margaret Bellatti Greulich WW, Thoms H. 1938. The dimensions of the pelvic inlet of 789 (Duckworth Collection, University of Cambridge) for white females. Anat Rec 72(1):45–51. access to collections instrumental to this study. We also Hallgrimsson B, Miyake T, Wilmore K, Hall BK. 2003. Embryological origins of developmental stability: size, shape and fluctuating asymmetry gratefully thank an anonymous reviewer for very con- in prenatal random bred mice. J Exp Zool B: Mol Dev Evol 296(1):40–57. structive comments on earlier drafts of the manuscript. Hallgrimsson B, Willmore K, Hall BK. 2002. Canalization, developmental stability, and morphological integration in primate limbs” Am J Phys LITERATURE CITED Anthropol 119(S35):131–158. Harrington Jr M, Keller T, et al., 1993. Geometric properties and the pre- Abel MF, Blanco JS, Pavlovich L, Damiano DL. 1999. Asymmetric hip dicted mechanical behavior of adult human clavicles. J Biomech 26(4): deformity and subluxation in cerebral palsy: an analysis of surgical 417–426. treatment. J Ped Orthopaed 19(4): 479–485. Husson, J-L, Mallet J-F, et al., 2010. The lumbar-pelvic-femoral complex: Abitbol MM. 1987. Obstetrics and posture in pelvic anatomy. J Hum Evol applications in spinal imbalance. Orthop Traumatol: Surg Res 96(4):S1– 16(3):243–255. S9. Abitbol MM. 1988. Evolution of the ischial spine and of the pelvic floor in Kelley JO, Angel JL. 1987. Life stresses of slavery. Am J Phys Anthropol the Hominoidea. Am J Phys Anthropol 75(1):53–67. 74(2):199–211. Al-Eisa E, Egan D, Deluzio K, Wassersug R. 2006. Effects of pelvic asym- Kibii JM, Churchill SE, Schmid P, Carlson KJ, Reed ND, De Ruiter DJ, metry and low back pain on trunk kinematics during sitting: a compari- Berger LR. 2011. A partial pelvis of Australopithecus sediba. Science son with standing. Spine 31(5): E135–E143. 333(6048):1407–1411. Anderson R. 1984. Misalignment in the Human Pelvis Measured on Radio- Krishan K, Kanchan T, DiMaggio JA. 2010. A study of limb asymmetry graphs. J Hum Evol 13(7):593–600. and its effect on estimation of stature in forensic case work. Forens Sci Angel JL. 1946. Skeletal change in ancient Greece. Am J Phys Anthropol Int 200(1):181. e181-181. e185. 4(1):69–98. Krogman WM. 1951. The scars of human evolution. Sci Am 185(6):54–57. Auerbach BM, Raxter MH. 2008. Patterns of clavicular bilateral asymme- Krukierek S. 1951. The sexual differences of the human pelvis. Gynecol try in relation to the humerus: variation among humans. J Hum Evol Obstet Invest 132(2):92–110. 54(5):663–674. Kurki HK. 2007. Protection of obstetric dimensions in a small-bodied Auerbach BM, Ruff CB. 2004. Human body mass estimation: a comparison human sample. Am J Phys Anthropol 133(4):1152–1165. of Morphometric and Biomechanical methods. Am J Phys Anthropol Kurki HK. 2011a. Pelvic dimorphism in relation to body size and body size 125(4):331–342. dimorphism in humans. J Hu Evol 61(6):631–643. Auerbach BM, Ruff CB. 2006. Limb bone bilateral asymmetry: variability Kurki HK. 2011b. Compromised skeletal growth? Small body size and clin- and commonality among modern humans J Hum Evol 50(2):203–218. ical contraction thresholds for the female pelvic canal. Int J Paleopath Badii M, Shin S, Torreggiani WC, Jankovic B, Gustafson P, Munk PL, 1(3):138–149. Esdaile JM. 2003. Pelvic bone asymmetry in 323 study participants Kurki HK. 2013a. Bony pelvic canal size and shape in relation to body pro- receiving abdominal CT scans. Spine 28(12):1335–1339. portionality in humans. Am J Phys Anthropol 151(1):88–101. Baltag V. 2009. Adolescent pregnancy: a culturally complex issue. Bull Kurki HK. 2013b. Skeletal variability in the pelvis and limb skeleton of World Health Org 87:410–411. humans: does stabilizing selection limit female pelvic variability? Am J Barber P. 2005. Contemporary views on female pelvic anatomy. Cleve Clin Hum Bio 25(6):795–802 J Med 72: S3. Kurki HK, Decrausaz S-L. 2016. Shape variation in the human pelvis and De Anna EB, Bonisoli-Alquati A, Mousseau TA. 2013. The use of fluctuat- limb skeleton: implications for obstetric adaptation. Am J Phys Anthro- ing asymmetry as a measure of environmentally induced developmental pol 159:88–101. instability: a meta-analysis. Ecol Indic 30:218–226. Latimer HB, Lowrance E. 1965. Bilateral asymmetry in weight and in Blackburn A. 2011. Bilateral asymmetry of the humerus during growth length of human bones. Anat Rec 152(2):217–224. and development. Am J Phys Anthropol 145(4):639–646. LaVelle M. 1995. Natural selection and developmental sexual variation in Blackburn A, Knusel CJ. 2006. Hand dominance and bilateral asymmetry the human pelvis. Am J Phys Anthropol 98(1):59–72. of the epicondylar breadth of the humerus: a test in a living sample. Lazennec JY, Brusson A, Rousseau MA. 2013. Lumbar-pelvic-femoral bal- Curr Anthropol 47(2):377–382. ance on sitting and standing lateral radiographs. Orthop Traumatol: Betti L, Cramon-Taubadel NV, Lycett SJ. 2012. Human pelvis and long Surg Res 99(1):S87–S103. bones reveal differential preservation of ancient population history and Leutenegger W. 1974. Functional aspects of pelvic morphology in simian migration out of Africa. Hum Biol 84(2):139–152. primates. J Hum Evol 3(3):207–222.

American Journal of Human Biology PELVIC AND CANAL ASYMMETRY 7

Levangie PK. 1999. The association between static pelvic asymmetry and Stock JT. 2006. Hunter-gatherer postcranial robusticity relative to pat- low back pain. Spine 24(12):1234–1242. terns of mobility, climatic adaptation, and selection for tissue economy. Lewton KL. 2012. Evolvability of the primate pelvic girdle. Evol Biol 39(1): Am J Phys Anthropol 131(2):194–204. 126–139. Tague RG. 1988. Bone resorption of the pubis and preauricular area in Lieberman DE, Devlin MJ, Pearson, OM. 2001. Articular area responses humans and nonhuman mammals. Am J Phys Anthropol 76(2):251–267. to mechanical loading: effects of exercise, age, and skeletal location. Am Tague RG. 1989. Variation in pelvic size between males and females. Am J J Phys Anthropol 116(4):266–277. Phys Anthropol 80(1):59–71. Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. 2003. Tague RG. 1991. Commonalities in dimorphism and variability in the Optimization of bone growth and remodeling in response to loading in anthropoid pelvis, with implications for the fossil record. J Hum Evol tapered mammalian limbs. J Exp Biol 206(18):3125–3138. 21(3):153–176. Lieberman DE, Polk JD, Demes B. 2004. Predicting long bone loading Tague RG. 1992. Sexual dimorphism in the human bony pelvis, with a con- from cross-sectional geometry. Am J Phys Anthropol 123(2):156–171. sideration of the Neandertal pelvis from Kebara Cave, Israel. Am J Phys Lovejoy CO. 2005. The natural history of human gait and posture: part 1. Anthropol 88(1):1–21. Spine and pelvis. Gait Post 21(1):95–112. Tague RG. 1994. Maternal mortality or prolonged growth: age at death Lovejoy CO, Suwa G, Spurlock L, Asfaw B, White TD. 2009. The pelvis and and pelvic size in three prehistoric Amerindian populations. Am J Phys femur of Ardipithecus ramidus: the emergence of upright walking. Sci- Anthropol 95(1):27–40. ence 326(5949):71–71e76. Tague RG. 1995. Variation in pelvic size between males and females in Manning JT. 1995. Fluctuating asymmetry and body weight in men and women: implications for sexual selection Ethol Sociobiol 16(2):145–153. nonhuman anthropoids. Am J Phys Anthropol 97(3):213–233. Mays S. 2002. Asymmetry in metacarpal cortical bone in a collection of Tague RG. 2000. Do big females have big pelves? Am J Phys Anthropol British post-mediaeval human skeletons. J Arch Sci 29(4):435–441. 112(3):377–393. Mays S, Cox M. 2000. Sex determination in skeletal remains. In: Mays S, Tague RG. 2007. Costal process of the first sacral vertebra: Sexual dimor- Cox M, editors. Human osteology in archaeology and forensic science. phism and obstetrical adaptation. Am J Phys Anthropol 132(3):395–405. Cambridge: Cambridge University Press. p 117–130. Tague RG, Lovejoy CO. 1986. The obstetric pelvis of AL 288-1 (Lucy). Mays S, Steele J, Ford M. 1999. Directional asymmetry in the human clav- J Hum Evol 15(4):237–255. icle. Int J Osteoarch 9(1):18–28. Tardieu C, Bonneau N, Hecquet J, Boulay C, Marty C, Legaye J, Duval- Moerman ML. 1981. A longitudinal study of growth in relation to body size Beaupe`re G. 2013. How is sagittal balance acquired during bipedal gait and sexual dimorphism in the human pelvis. Anna Arbor, MI: Univer- acquisition? Comparison of neonatal and adult pelves in three dimen- sity of Michigan. sions. Evolutionary implications. J Hum Evol 65(2):209–222. Moller A, Manning J. 2003. Growth and developmental instability. Vet J Timgren J, Soinila S. 2006. Reversible pelvic asymmetry: an overlooked 166(1):19–27. syndrome manifesting as scoliosis, apparent leg-length difference, and Nicholson C. 1945. The two main diameters at the brim of the female pel- neurologic symptoms. J Manipulative Physiol Ther 29(7):561–565. vis. J Anat 79(3):131. Tomkinson GR, Olds TS. 2000. Physiological correlates of bilateral symme- Palmer AR, Strobeck C. 1986. Fluctuating asymmetry: measurement, try in humans. Int J Sports Med 21(8):545–550. analysis, patterns. Annu Rev Ecol Syst 17(1):391–421. Walker AP, Dickson RA. 1984. School screening and pelvic tilt scoliosis. Phenice TW. 1969. A newly developed visual method of sexing the os pubis. Lancet 324(8395):152–154. Am J Phys Anthropol 30(2):297–301. Walrath DE, Glantz MM. 1996. Sexual dimorphism in the pelvic midplane Plochocki JH. 2002. Directional bilateral asymmetry in human sacral mor- and its relationship to Neandertal reproductive patterns. Am J Phys phology. Int J Osteoarch 12(5):349–355. Anthropol 100(1):89–100. Plochocki JH. 2004. Bilateral variation in limb articular surface dimen- Washburn SL. 1948. Sex differences in the pubic bone. Am J Phys Anthro- sions. Am J Hum Biol 16(3):328–333. pol 6(2):199–208. Rak Y, Arensburg B. 1987. Kebara 2 Neanderthal pelvis: first look at a Washburn SL. 1949. Sex differences in the pubic bone of Bantu and Bush- complete inlet. Am J Phys Anthropol 73(2):227–231. man. Am J Phys Anthropol 7(3):425–432. Rosenberg K, Trevathan W. 1995. Bipedalism and human birth: the obstet- Washburn SL, Sahlins MD, et al., 1960. The human species. Biodemogra- rical dilemma revisited. Evol Anthropol: Issues News Rev 4(5):161–168. phy Soc Biol 7(4):217–225. Rosenberg K, Trevathan W. 2002. Birth, obstetrics and human evolution. Weaver TD, Hublin J-J. 2009. Neandertal birth canal shape and the evolu- BJOG 109(11):1199–1206. tion of human childbirth. Proc Natl Acad Sci U S A 106(20):8151–8156. Rosenberg KR. 1992. The evolution of modern human childbirth. Am J Phys Anthropol 35(S15):89–124. Wells C. 1975. Ancient obstetric hazards and female mortality. Bull N Y Rosenberg KR. 1988. The functional significance of Neandertal pubic Acad Med 51(11):1235. length. Curr Anthropol 29(4):595–617. Wells JC, DeSilva JM, Stock JT. 2012. The obstetric dilemma: an ancient Ruff, C. 2010. Body size and body shape in early hominins–implications of game of Russian roulette, or a variable dilemma sensitive to ecology? the Gona Pelvis. J Hum Evol, 58(2):166–178. Am J Phys Anthropol 149(S55):40–71. Schultz AH. 1930. The skeleton of the trunk and limbs of higher primates. Wittman AB, Wall LL. 2007. The evolutionary origins of obstructed labor: Hum Biol 2(3):303–438. bipedalism, encephalization, and the human obstetric dilemma. Obstet Schultz AH. 1949. Sex differences in the pelves of primates. Am J Phys Gynecol Surv 62(11):739–774. Anthropol 7(3):401–424. World Health Organization. 2005. The World Health Report 2005: Make Schutz H, Donovan ER, Hayes JP. 2009. Effects of parity on pelvic size and every mother and child count, World Health Organization. shape dimorphism in Mus. J Morph 270(7):834–842. World Health Organization. 2012. Trends in maternal mortality: 1990 to Steele J, Mays S. 1995. Handedness and directional asymmetry in the 2010: WHO, UNICEF, UNFPA and The World Bank estimates, World long bones of the human upper limb. Int J Osteoarch (1):39–49. Health Organization.

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