Skeletal variability in the pelvis and limb skeleton of humans: Does stabilizing selection limit female pelvic variation?

Original Research Article

Skeletal Variability in the Pelvis and Limb Skeleton of Humans: Does StabilizingSelection Limit Female Pelvic Variation?

HELEN K. KURKI*Department of Anthropology, University of Victoria, Victoria, British Columbia, Canada V8W 2Y2

ABSTRACT: Objectives: This study tests the hypothesis, a correlate of the obstetric dilemma, that skeletal vari-ability in the human female pelvic canal is limited owing to the action of stabilizing selection. Levels of variation inthree skeletal regions (pelvic canal, noncanal pelvis, and limbs) of females and males are compared to each other andbetween sexes.

Methods: Nine human skeletal samples (total female n 5 101; male n 5 117) representing diverse populations wereincluded. Osteometric data were collected from the articulated pelvis, os coxa, sacrum, femur, tibia, humerus, radius,and clavicle. Coefficients of variation, adjusted for small sample size (V*), were calculated for variables in separatesamples by sex, and mean V*s were taken for the skeletal regions. Size variances were measured as V* of the geometricmean (GM) of the skeletal region variables. Using nonparametric methods, coefficients were compared between sexesand skeletal regions and correlations among V*s were calculated.

Results: Females and males do not differ in levels of variation for any skeletal region. The pelvic canal is the mostvariable region in both sexes, while size variability (GM) is similar among the three skeletal regions. Across the sam-ples, canal and noncanal pelvic regions share patterns of variability in females but not males, while variability of thelimb skeleton is independent in both sexes.

Conclusions: The results suggest that stabilizing selection does not limit variability in the female pelvic canal. Bio-logical plasticity may be greater in the canal than that in other skeletal regions. Am. J. Hum. Biol. 25:795–802, 2013.VC 2013 Wiley Periodicals, Inc.

The pelvic canal of humans displays differences in sizeand shape between females and males, presumably owingto its differential functional roles in locomotion andobstetrics. The obstetric dilemma (OD) hypothesis (Wash-burn, 1960) has been the predominant evolutionary modelfor the human pelvis. Under this model the risk and painthat accompany human childbirth and the altriciality ofthe human neonate result from both the biomechanicalconstraints of bipedal locomotion (narrow distancebetween hip joints) and obstetrics (birthing a relativelylarge-brained neonate). Given the risk of obstructed labordue to the close fit between the size of the maternal canaland the size of the neonatal head and shoulders, whichcan result in cephalo-pelvic disproportion, childbirth isviewed as a time of significant mortality risk for bothmother and neonate. As such, strong selective pressuresare believed to act on the female pelvis to ensure success-ful childbirth, thereby limiting pelvic canal variability asa result of stabilizing selection on canal morphology. In arecent reevaluation of the OD, Dunsworth et al. (2012)have argued that energetics of gestation and growth,rather than biomechanical factors, contribute to gestationlength and neonatal maturity. The biomechanical predic-tion of the OD that the wider pelvic breadth of femalesputs them at a locomotory disadvantage has also beenquestioned. Warrener and coworkers (Dunsworth et al.,2012; Warrener, 2012, 2013) have shown that males andfemales do not differ in locomotor cost despite dimorphismin aspects of lower limb bone and muscle structure, inpart because variations in the dynamics of gait betweenthe sexes accommodate these differences. Similarly, Wellset al. (2012) challenge the perception of risk in childbirthunder the OD, suggesting instead that historical periodsof resource stress have inflated the prevalence ofobstructed labor due to differential plasticity in maternal

body size and pelvic capacity, and neonatal size. Thesestudies suggest that the evolution of the human pelvismay not have been as simple as predicted by the ODhypothesis.

Levels of phenotypic variability in a species are depend-ent on the interaction between plasticity—the ability ofan organism to adapt during growth to stimuli—and con-straint—genetic, developmental, and selective limitationson morphology (Buck et al., 2010; Grabowski, 2013).Greater plasticity results in greater intraspecific variabil-ity, whereas greater constraint reduces it. Although intra-specific variation is the raw material for natural selection,canalization of structures reflects constraint imposed byprocesses such as stabilizing selection (Flatt, 2005; Wad-dington, 1942). Intraspecific variation can be classed intointrinsic character variation (intrapopulation variation),intersexual variation (sexual dimorphism), and interpo-pulation variation due to local adaptations or temporallyspecific selective environments (Plavcan, 2012). Intrinsiccharacter variation can be generated by genetic or envi-ronmental influences (Plavcan, 2012), the latter repre-senting phenotypic plasticity. Dissimilar levels ofphenotypic variability in discrete skeletal regions can

Additional Supporting Information may be found in the online versionof this article.

Contract grant sponsor: Social Sciences and Humanities Research Coun-cil of Canada; Contract grant number: 410-2008-2344.

*Correspondence to: Helen Kurki, Department of Anthropology, Univer-sity of Victoria, PO Box 1700 STN CSC, Victoria, BC, Canada V8W 2Y2.E-mail: [email protected]

Received 20 June 2013; Revision received 16 August 2013; Accepted 19August 2013

DOI: 10.1002/ajhb.22455Published online 7 October 2013 in Wiley Online Library

(wileyonlinelibrary.com).

VC 2013 Wiley Periodicals, Inc.

AMERICAN JOURNAL OF HUMAN BIOLOGY 25:795–802 (2013)

mailto:[email protected]

indicate varying actions of selection acting on theseregions. Regions with low variability may be constrainedby stabilizing selection owing to functional or develop-mental requirements, whereas regions with high variabil-ity may be more plastic and therefore responsive toenvironmental stimuli (Buck et al., 2010; Maynard Smithet al., 1985), or may be subject to relaxed selection pres-sures. If the pelvis, specifically the pelvic canal, was con-strained under the influence of stabilizing selection, wewould expect this skeletal region to display lower intra-specific (and intrapopulation) variability than other skele-tal regions.

Contrary to expectations under stabilizing selection,Tague (1989) demonstrated that females are not less vari-able than males in dimensions of the pelvic canal. In hisstudy, coefficients of variation (CVs) of pelvic dimensionswere compared individually (e.g., inlet anteroposterior,inlet transverse diameter, etc.). Several skeletal sampleswere examined individually, including both moderncadaveric and archaeological samples from North Amer-ica; no consistent differences in variation between femalesand males were found within these samples. In a laterstudy, Tague (1995) expanded his examination of sex-specific pelvic variability to nine other anthropoid species,with generally similar results. These two studies suggestthat stabilizing selection may not act to limit variability ofpelvic canal dimensions in females specifically, relative tomales. Meanwhile, LaVelle (1995) examined sex differen-ces in variation in the growing pelvis in a longitudinalstudy, specifically focused on changes in coefficients withage (between ages 8 and 18 years). She found that femalesand males at 8 and 18 years do not differ significantly invariation of linear pelvic dimensions, but changes in vari-ation did occur in both sexes in several dimensionsbetween these ages. Some dimensions showed concord-antly reduced variation, indicative of growth canalizationin both sexes. Others showed discordant changes in varia-tion between the sexes. LaVelle proposed that these pat-terns are indicative of stabilizing and disruptive selection,respectively. Yet, sexual dimorphism in the pelvis,whereby females possess larger pelvic canal dimensions(for body size) than males, contra dimorphism in otheraspects of body size (e.g., stature, body mass, and nonpel-vic skeletal structures), is most parsimoniously explainedas resulting from selection for obstetric sufficiency infemales (Kurki, 2011a; Leutenegger, 1974; Leuteneggerand Larson, 1985; Schultz, 1949; Tague, 1992; Trevathanand Rosenberg, 2000; Wood and Chamberlain, 1986).Betti et al. (2012, 2013) have detected the influence ofdrift in producing patterns of variation in pelvic morphol-ogy among human populations, further complicating therole of selection. Together, these studies suggest a complexinterplay of selection, both stabilizing and disruptive, andgenetic drift influencing pelvic variation in humans. But,what role does developmental plasticity play in thisprocess?

The relationships among pelvic canal shape and sizeand various aspects of body size and shape have beenshown to vary among human populations (Kurki, 2007,2013a), implying that the pelvis may be more plastic ormore evolvable within the human species than a simplescenario of selection contrasting locomotor and obstetricdemands might imply. Previous research (Kurki, 2013a)established that some aspects of the shape of the canalwere correlated with body breadth and body mass (heav-

ier, broader bodies displayed broader pelvic canals) acrossher nine skeletal samples; yet several female samples dis-played sample-specific canal shapes. Contrasting canalshapes were evident between the South African, AfricanPygmy, and Fuegian females versus the North Africans,Australians, and Danes—all samples that varied in bodysize and shape characteristics. The South African femalesin particular seem to display a uniquely shaped canal.Similar sample-specific canal shapes were not seen amongthe males. These results are consistent with the notionthat the pelvis of humans is particularly evolvable, thatis, highly able to evolve in the direction of selection withlow genetic constraints (Grabowski, 2013; Grabowskiet al., 2011), or that pelvis is particularly responsive tovariations in health, locomotion, and energetics amongother factors (Wall-Scheffler, 2012a,b; Wells et al., 2012).Recent studies (Grabowski, 2013; Grabowski et al. 2011;Lewton, 2012) have investigated modularity and morpho-logical integration (levels of association between traits) inthe pelvis of primate species. Grabowski (Grabowski,2013; Grabowski et al., 2011) has shown that the humanos coxa and obstetric canal are less morphologically inte-grated in humans than African apes, meaning thatgenetic constraints on the birth canal related to otheraspects of the pelvis are reduced in humans. This indi-cates that more of the variation that is present in thetraits of the human obstetric canal is available for naturalselection to act on; the human canal has higher evolvabil-ity than those of other apes. Less constraint may thereforeenable greater variability and perhaps greater plasticity.Further, the lack of an association between sexual dimor-phism of the pelvis and of body size (Kurki, 2011a) maysupport an expectation of dissimilar variability in pelvicand nonpelvic regions. How variable then is the pelviccanal as a whole relative to other skeletal regions? Byexamining intrapopulation variation in human popula-tions, this study compares levels of human phenotypicvariability in the pelvic canal, the noncanal aspects of thepelvis, and the appendicular skeleton to test the assump-tion that obstetric selection constrains the variability ofthe pelvic canal relative to these other skeletal regions,and in females relative to males.

Under the assumption that obstetric selection acts onthe female pelvic canal to ensure size characteristicsadequate for childbirth, the following predictions weremade: (1) females will be less variable in the canal andnoncanal aspects of the pelvis than males, for bothregional variation and size variation, whereas variationin the appendicular skeleton is not expected to differbetween the sexes; (2) the pelvic canal will be the leastvariable anatomical region in both females and males,whereas the appendicular skeleton will be the most vari-able region in both sexes; and (3) a similar pattern ofbetween-region variability will be present for size (low incanal and higher in pelvis and limbs).

MATERIALS AND METHODS

Nine skeletal samples (Table 1) representing a range ofcharacteristic body sizes and shapes (Kurki, 2013a) wereincluded in this study (total female n 5 101; malen 5 117). All skeletons were determined to be adult (iliaccrest at least beginning fusion), and sex was estimatedbased on osteological features of the pelvis, and wherepossible, the cranium (Buikstra and Ubelaker, 1994).

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Osteometric data (Fig. 1 and Table 2) were collected fromthe os coxa, articulated pelvis, femur, tibia, humerus,radius, and clavicle. Bilateral measurements were aver-aged from right and left sides when both sides were avail-able. The pelvis was articulated without accommodationsfor the soft tissue at the pubic symphysis and sacroiliacjoints that would be present in life. Bonneau et al. (2012)have shown that variation among individuals in theamount of soft tissue at these joints has minimal effect onmeasurements of the pelvis.

Three classes of variables (Table 2) were created to cap-ture variation within canal, noncanal pelvic, and appen-dicular regions. Coefficients of variation (CV 5 standarddeviation/mean*100) were calculated for each variableseparately for each sample and sex; CVs were converted

to V* to accommodate small samples sizes [V* 5 (1 11/4n)*CV] (Sokal and Rohlf, 1995). These coefficients pro-vide a size-free means of examining levels of variation.Mean V*s were calculated for each measurement class.Variability in shape of the skeletal regions may tend toincrease the variation of the individual dimensions of ameasurement class, resulting in high V* values; there-fore, it is also of interest to compare size variation, partic-ularly if there is a relationship between pelvic canalcapacity and risk of obstructed labor. To capture variabili-ty of overall size for each skeletal region, the geometricmean (GM) of the measurements in each class was calcu-lated (Mosimann, 1970), and mean V*s of GMs for eachskeletal region were taken. GM is a common size measurefor studies of skeletal variation (Coleman, 2008; Royeret al., 2009; Silverman et al., 2001). Mean V* for the vari-able class of a particular skeletal region and the V* of theGM for that region are expected to be highly correlated,but GM V* will be less affected by shape variation in theskeletal region within the sample. As Coleman (2008) hasdetermined, the CV of a GM of multiple measurements isconsistently lower than the CV of an individual measure-ment, therefore GM and class V*s cannot be directly com-pared. It was also anticipated that GM V*s would belower than variable class V*s.

Differences in V*s were tested to address the followingquestions: (1) are there differences between the sexes inthe levels of variation for each skeletal region, and (2)within each sex, are there differences between the skele-tal regions (including size) in the levels of variation? Dif-ferences between the sexes for each skeletal region wereexamined using Mann–Whitney U-tests; differenceswithin each sex between skeletal regions were examinedusing Wilcoxon signed-rank tests. Spearman correlation

TABLE 1. Details of skeletal samples included in this study

Sample Date Institution

African Pygmy 20th century IRSN, MdH, UGAndaman Islands ca. 1860–1900 AMNH, DC, NHMPhilippines 19th century MdHSouth Africa 240–5370 BP (14C)a ALM, IMCT, NMB, UCTNorth Africa 2000 BC–AD 550 AMNH, DC, UCOPAustralia 19th century MdH, NHM, UGDenmark Medieval UCOPTierra del Fuego ca. 1880 MAE, MdH, URInuit AD 800–1900 AMNH, CMC

ALM, Albany Museum; AMNH, American Museum of Natural History; CMC,Canadian Museum of Civilization; MdH, Musee de l’Homme; DC, DuckworthCollection, University of Cambridge; IMCT, Iziko Museums of Cape Town;IRSN, Institut Royal des Sciences Naturelles de Belgique; MAE, Museo di Antro-pologia e Etnologia, Universit�a degli Studi di Firenze; NHM, Natural HistoryMuseum; NMB, National Museum, Bloemfontein; UCOP, University of Copen-hagen; UCT, University of Cape Town; UG, Universit�e de Geneve; UR, Museo diAntropologia, Universit�a di Roma.aUncalibrated radiocarbon dates.

Fig. 1. Pelvic measurements used in this study (see also Table 2).

SKELETAL VARIABILITY OF THE PELVIS AND LIMBS 797


coefficients were calculated between V*s to examine pat-terns of correlation in variability among the variableclasses and GMs. Nonparametric tests were used to testfor differences and for the correlation analyses becausesample sizes are small (N 5 9 for both sexes). Statisticalanalyses were conducted using PAST 2.17 statistical soft-ware (Hammer et al., 2001).

The samples included in this study are principally fromarchaeological contexts to enable tighter control on thespatial and genetic parameters of the populations repre-sented. Although modern cadaveric or anatomical skeletalcollections may have provided larger sample sizes, theintrapopulation variation would have been increasedowing to the mixture of populations represented. The con-dition of the skeletons was variable, resulting in some rel-atively small individual sample sizes as well as disparityin sample sizes for each skeletal region (see SupportingInformation Table S1); only individuals preserving allmeasurements in a given class were included in the sam-ple for that variable set as the calculation of GMs for eachclass requires no missing data. No females from the Fue-gian sample preserved all the limb measurements; there-fore, mean V*s for the remaining eight samples were usedin to fill the missing values for the limbs variable class.Some of the samples are small, but include all skeletonsavailable for study; therefore, caution must be taken inassuming representativeness of these populations. None-theless, these samples were chosen because they each rep-resent a relatively confined population in time and space,and together they capture a wide range of human bodysizes and shapes. Separate analyses (Kurki, 2013b) com-paring only mean V* for each variable class (not includingGM) using all specimens that preserve at least one mea-

surement per variable class produce the similar results,with one exception, which is discussed in the Resultssection.

RESULTS

The results of the Mann–Whitney U-tests (Table 3) indi-cate that females and males do not differ for variable classV*s or GM V*s. This is somewhat different from an earlieranalysis (Kurki, 2013b) that only examined the threevariable class V*s (GM was not included), and thereforecomprised larger samples as individuals missing one ormore of the measurements in a region were retained. Inthe previous study, males were more variable in the limbskeleton than females (male limb V* 5 6.16; female limbV* 5 5.25; Mann–Whitney P 5 0.038). The restricted sam-ples for this study have therefore altered to some degreethe variability of measurement classes (see SupportingInformation). The Wilcoxon signed-rank tests (Table 4)between variable classes show similar results for bothsexes. The pelvic canal is significantly more variableacross the samples than the noncanal aspects of the pelvisand the limb skeleton, whereas the noncanal pelvis is notmore variable than the limb skeleton. The GM V*s are notsignificantly different among the three skeletal regions(Table 4). Figure 2 illustrates the distribution of sampleV*s by sex for each skeletal region.

To examine relationships in variability among the skele-tal regions, Spearman correlation coefficients were calcu-lated (Table 5) separately for each sex. As expected, classand GM variations are highly correlated. The more inter-esting relationships are those between the different regionsand GMs. Males display fewer significant relationships

TABLE 2. Descriptions of measurementsa used in this study (see also Fig. 1)

Measurement Description

Canal variable classInlet anteroposterior Sacral promontory to dorsomedial superior pubis (A, Fig. 1)Inlet transverse Maximum distance between linea terminalis (B)Inlet anterior length Curved length of linea terminalis from INML to dorsomedial superior pubis (C)Inlet posterior length Curved length of linea terminalis from INML to apex of auricular surface (D)Midplane anteroposterior From junction of fourth and fifth sacral vertebrae to dorsomedial inferior pubis (E)Midplane transverse Between ischial spines (F)Midplane anterior length Ischial spine to dorsomedial inferior pubis (G)Midplane posterior length S4–S5 junction to ischial spine (H)Outlet anteroposterior Apex of fifth sacral vertebrae to dorsomedial inferior pubis (I)Outlet transverse Distance between inner margins of transverse ridge of ischial tuberosities (J)Outlet anterior length Transverse ridge of ischial tuberosity to dorsomedial inferior pubis (K)Outlet posterior length Apex of S5 to transverse ridge of ischial tuberosity (L)Pelvis variable classBi-iliac breadth Maximum distance across the right and left iliac blades (M)Biacetabular breadth Distance between acetabulae (N)Os coax length From most superior point on iliac crest to most inferior point of ischial tuberosity (O)Iliac height From Schultz’s Point Ab to most superior point on iliac crest (P)Iliac breadth Distance between anterior superior and posterior superior iliac spines (Q)Ischial length From Schultz’s Point A to transverse ridge of ischial tuberosity (R)Pubic bone length From Schultz’s Point A to superior aspect of symphyseal face (S)Sacral breadth Maximum breadth of anterior sacrum (T)Limbs variable classFemoral length Maximum length measured from proximal head to distal condylesFemoral head diameter Maximum diameter of the femoral headTibial length Maximum length including the spines, measured to the lateral condyleHumeral length Maximum length measured from proximal head to distal trochleaRadial length Maximum length measured from proximal head to distal styloid processClavicular length Maximum length medial to lateral extensions

aMeasurement definitions are from Tague (1989), Buikstra and Ubelaker (1994), and Kurki (2007, 2013a).bSchultz’s Point A is at the fusion point in the acetabulum of the three elements of the os coxa, characterized by a notch and irregular bone.

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among the skeletal regions than females. Variation in thecanal is highly correlated with variation in the noncanalaspects of the pelvis (pelvis and pelvis GM) in the femalesonly. Variation in the limbs (limbs and limbs GM) is notrelated to variation in either the canal or noncanal pelvisin both sexes. In general then, it appears that factors thatinfluence variation (i.e., plasticity) in the pelvis are distinctfrom those influencing variation in the limbs. Further, var-iability in the canal and noncanal pelvis is more interre-lated in females than in males.

DISCUSSION

Under a hypothesis of conflicting selective pressuresrelating to obstetric function and bipedalism in females(for discussion, see Dunsworth et al., 2012; Wall-Scheffler,2012a), it was anticipated that measurements of the pel-vic canal would display low variability in females relativeto males, as males would be free to vary more in responseto developmental, functional, or environmental factorsthan females. The lack of sex-based differences in vari-ability measures of the pelvis (both canal and noncanal)and limbs skeleton suggests this is not the case across thestudy samples. If high variability in skeletal dimensions

reflects high plasticity in response to environmental sig-nals, it was further expected that in comparisons withnoncanal pelvis and appendicular variability the pelviccanal would display low variability in both sexes. Thisexpectation was also not met in this study. These resultswere not anticipated for the same reasons, that is, obstet-ric selection was expected to act to constrain variability ofthe pelvic canal in females, and in males via a correlatedresponse. Instead, the canal is the most variable of theanatomical regions. Yet, in the comparisons of size varia-tion (GM V*s), there are no differences in variance amongthe skeletal regions. Although the class and GM V*s arenot directly comparable owing to the influence on varia-tion of the GM calculation (Coleman, 2008), these resultssuggest that overall canal “size” varies less than canal“shape” within these populations because the “size” com-ponent extracted as the GM from the measurements ineach class is intended to exclude elements of “shape” vari-ation among linear dimension raw data.

The results of this study may be explained if the pelvisresponds plastically to environmental stimuli, but morespecifically that pelvic canal shape is more affected thanis size within a population. Obstetric capacity may be pro-tected, to enable a sufficiently sized canal to birth a largeneonate, by expanding the canal in some dimensions (e.g.,anterior-posterior length) to accommodate reductions inother dimensions (e.g., transverse length). This plasticityin canal shape would result in elevated levels of variabili-ty for size dimensions of the pelvic canal within a popula-tion, as are found here. That is, each particular canalmeasurement would display a high CV. Plasticity in canalshape, rather than in overall capacity (size), in this man-ner is consistent with the observation that some, but notall, populations appear to display characteristic aspects ofcanal shape (Kurki, 2013a). A relatively plastic pelviccanal also accords with the pelvic plasticity model pre-sented by Wells et al. (2012), who argue that the magni-tude of OD may be more sensitive to ecological pressuresacting over shorter time frames than selection on pelvic

TABLE 3. Mean V* for variable classes and geometric means by sample and sex and Mann–Whitney U-tests for differencesin V*s between the sexes

Canal GMa n Pelvis GM n Limbs GM n

African Pygmy Female 6.67 3.86 6 5.11 4.28 6 3.75 3.05 5Male 8.23 3.63 6 5.83 5.09 6 5.04 4.41 5

Andaman Islands Female 6.41 4.46 3 5.56 4.10 6 4.99 3.54 4Male 9.64 7.44 5 7.71 6.95 5 3.68 2.87 4

Philippines Female 8.02 5.98 6 5.17 4.49 8 4.23 3.14 6Male 9.14 4.48 4 9.40 8.19 8 5.87 5.52 5

South Africa Female 9.71 6.94 9 7.22 5.74 15 6.48 5.67 14Male 9.64 7.44 10 7.85 6.36 14 6.56 5.69 9

North Africa Female 7.87 5.53 9 5.71 3.91 17 4.69 3.59 15Male 8.57 5.77 15 5.06 3.74 22 7.70 6.96 18

Australia Female 10.13 7.22 6 7.48 5.87 8 4.36 3.90 4Male 9.14 4.48 8 4.42 2.92 8 5.79 4.53 8

Denmark Female 6.87 0.31 3 4.70 3.31 7 7.16 5.98 5Male 8.23 3.63 7 4.56 3.47 8 4.62 3.94 5

Tierra del Fuego Female 4.98 2.95 6 4.55 3.23 9 5.16b 4.23b 0Male 9.18 5.06 11 4.93 3.82 14 6.79 5.87 5

Inuit Female 8.76 6.70 9 5.57 4.15 25 5.63 4.97 24Male 8.57 5.77 18 5.09 3.93 32 5.10 3.79 30

Mean of female samples 8.27 4.65 9 5.15 3.83 9 5.89 4.99 9Mean of male samples 8.24 4.53 9 5.16 3.84 9 5.67 4.75 9Mann–Whitney P-value 0.102 0.757 0.965 0.825 0.310 0.270

aGM 5 geometric mean of measurements in variable class.bNo female Fuegian skeletons preserve all the variables in the limbs skeletal region; therefore, the mean limbs V*s across the remaining eight samples are used forthe female Fuegians.

TABLE 4. Wilcoxon signed-rank tests for differences in mean V*sbetween variable classes, sexes separate

Comparison

Females Males

z P-value z P-value

Canal vs. pelvis 2.67 0.008 2.55 0.011Canal vs. limbs 2.31 0.021 2.67 0.008Pelvis vs. limbs 1.24 0.214 0.18 0.859Canal GM vs. pelvis GM 1.13 0.260 1.01 0.314Canal GM vs. limbs GM 1.13 0.260 0.18 0.859Pelvis GM vs. limbs GM 0.53 0.594 0.18 0.859

Significant results (P<0.05) are indicated in bold.



dimensions or neonatal size. This study adds to the cur-rent discussions examining the assumptions behind theOD, that is, the relative importance of obstetric selectionin constraining the female pelvis and neonatal size inhumans (e.g., Dunsworth et al., 2012; Wells et al., 2012).It is important to note, however, that although theassumption underlying the study predictions has beenthat the female pelvis is under stabilizing selection(obstetrics and locomotor), but the male pelvis is not, it ispossible that selection is not relaxed on males, but acts inmultiple directions on the pelvis, such as to subject malesto stabilizing selection as well. If there are sex-based dif-ferences in the consequences of locomotor fitness, males

may be subject to just as high selective pressures asfemales. This scenario, though not possible to test here,would explain the similar levels of pelvic variationbetween the sexes.

Additional considerations can be derived from recentexaminations of the effect of drift on human postcranialmorphology. Betti et al. (2012, 2013) investigated patternsof within- and between-population phenotypic variationin the os coxa. Their results provide an important frame-work for considering the role of selection versus neutralevolutionary processes (e.g., drift) acting on the pelvis.Several key findings are relevant in the context of thisstudy. Betti et al. (2012, 2013) find greater within- than

Fig. 2. Boxplot of distributions of sample mean V*s for variable classes and GMs, separated by sex. Median value indicated by the line insidethe box, box extends from the 25th to 75th percentiles, whiskers extend from 2.5th or minimum value to 97.5th or maximum value, circles indi-cate outliers.

TABLE 5. Spearman correlation coefficientsa for females (right, n 5 9) and males (left, n 5 9)

Canal Canal GM Pelvis Pelvis GM Limbs Limbs GM

Canal r – 0.83 0.82 0.78 0.03 0.27P-value 0.002 0.007 0.013 0.932 0.488

Canal GM r 0.74 – 0.90 0.83 20.15 0.02P-value 0.022 0.001 0.005 0.700 0.966

Area r 0.86 0.95 0.72 0.67 20.12 20.17P-value 0.003 <0.001 0.030 0.050 0.765 0.966

Pelvis r 0.37 0.39 – 0.70 20.07 0.07P-value 0.323 0.300 0.036 0.865 0.865

Pelvis GM r 0.43 0.36 0.97 – 20.38 20.22P-value 0.245 0.335 <0.001 0.308 0.576

Limbs r 0.21 0.23 20.02 20.13 – 0.93P-value 0.584 0.554 0.966 0.732 <0.001

Limbs GM r 0.14 0.06 20.05 20.17 0.95 –P-value 0.711 0.879 0.898 0.668 <0.001

Significant correlations (P<0.05) indicated in bold.

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between-population variation in the os coxa, which is con-sistent with neutral evolutionary processes, as is seen inthe cranium (Betti et al., 2010; Roseman and Weaver,2004; von Cramon-Taubadel, 2009), and contrasting withtraits such as skin color, believed to be under strong selec-tive pressure. Within-population phenotypic variation inthe os coxa decreases with distance from the hypothesizedgeographical origin of humans, a pattern consistent withan Out of Africa dispersal model (Betti et al., 2013). Theseresults imply that selection acting on the pelvis may beless constraining of os coxa shape than predicted underthe OD hypothesis. However, the authors detected lowervariation in shape of the true pelvis (as represented intheir study by lower os coxa shape) versus the false pelvisin both sexes, indicating some influence of selection actingon the true pelvis (Betti et al., 2013). They suggest thefact that both sexes showed similar results indicates thatfemale true pelvis shape is not differentially influenced byselection, males and females are equally affected. Thelack of sex-based differences in canal and pelvis variabili-ty in this study is consistent with this latter finding, sug-gesting that females are not differentially constrainedrelative to males in pelvic variation. Yet, contrary to thesefindings, the results of this study indicate that the canalis more variable than the noncanal aspects of the pelvis.It is important to note, however, that Betti et al. examinedshape variation (landmark data) in three-dimensionalspace, whereas this study examines variation of lineardimensions, which do not capture shape of the morpholog-ical structures, only size of dimensions. Further, Bettiet al. included landmarks representing shape of the oscoxa specifically, whereas this study considered the articu-lated pelvis as a whole. These differences may indicatethat variation in the canal is increased by variation in thepositioning of the sacrum relative to the os coxa, resultingin size and shape variation in the whole pelvis that is notcaptured on the os coxa alone.

It is not the intention here to argue that selection doesnot act through pregnancy and childbirth. Given the cen-tral place of reproduction to the action of natural selec-tion, pregnancy and childbirth are clearly periodstargeted by selection acting both on the mother and theneonate. Several examples of metabolic, physiological,and immune response candidate genes under selectionthrough pregnancy have been identified (Brown et al.,2013), as well as energetic factors relating to mother andfetus (Dunsworth et al., 2012). The interactions of needsrelating to reproduction and mobility, during gestationand after, are also relevant in a selective context (Kramer,1998; Trevathan and Rosenberg, 2000; Wall-Scheffler,2012a,b; Wall-Scheffler and Myers, 2013; Wall-Scheffleret al., 2007; Watson et al., 2008). Nor is it likely thatobstetrical selection plays no role in the morphology of thepelvic skeleton of human females, given the pattern ofsexual dimorphism observed (Kurki, 2011a; Leutenegger,1974; Leutenegger and Larson, 1985; Schultz, 1949;Tague, 1992; Trevathan and Rosenberg, 2000; Wood andChamberlain, 1986), though alternative explanations forthe relatively large pelvic canal of females have been pro-posed (Schultz, 1949; Tague, 2005). The results presentedhere highlight the complexity of processes acting on skele-tal morphology and further question the explanatorypower of the OD hypothesis, whereby stabilizing selectionacts on the pelvis through obstetric versus locomotor fac-tors. Rather, it appears that flexibility in response to envi-

ronmental stimuli is the key to the development of pelvicmorphology, enabling the pelvis to be obstetrically suffi-cient under normal circumstances. Given the linkbetween maternal stature and perinatal mortality, thedetriment of this plasticity may then be apparent whenconditions during growth are insufficient leading to exac-erbation of the OD, that is, increasing the risk of cephalo-pelvic disproportion (e.g., Kurki, 2011b; Wells et al.,2012). The questions therefore become: how does thisplasticity in pelvic form relate to the low morphologicalintegration and high evolvability of the pelvis as illus-trated by Grabowski et al. (2011; Grabowski, 2013)? Is thehuman pelvis also then more plastic than that of otherprimate species? What factors influence the form of thepelvis during growth in an environment that is not nutri-tionally or health compromised (e.g., activity, diet, andgenetics)?

CONCLUSION

Recent research has focused extensively on addressingthe evolution and morphology of the human pelvis, includ-ing factors influencing its form (Betti et al., 2012, 2013;Wall-Scheffler, 2012a,b; Wells et al., 2012), relationshipsto body size and shape (Kurki, 2007, 2013a; Tague, 2000),patterns of sexual dimorphism (Kurki, 2011a; Tague,2005), and the levels and patterns of morphological inte-gration and evolvability relative to other primates (Gra-bowski, 2013; Grabowski et al., 2011; Lewton, 2012).These studies, along with an increased focus on the evolu-tion of hominin childbirth processes (e.g., DeSilva, 2011;Dunsworth et al., 2012; Weaver and Hublin, 2009), seekto comprehend and explain the uniqueness, or not, ofhuman childbirth and the morphological and physiologi-cal constraints acting on mother and child. The ODhypothesis, which pits the functional requirements ofbirthing large-brained (but altricial) babies againstbipedal locomotion as factors determining pelvic form andneonatal size, has been the predominant paradigm sincethe mid-20th century. Under this hypothesis, variation inthe pelvis, particularly in the pelvis of human females,was expected to be relatively low compared with malesand with noncanal aspects of the pelvis and the appendic-ular skeleton. Although the former were expected to beconstrained in form by stabilizing selection, the latterwere expected to be free to vary in form, as they are notunder these constraints. However, none of these expecta-tions were upheld with the sample in this study. Femalesand males do not differ in levels of variation in any of theskeletal regions examined, nor is the canal the least vari-able skeletal region. Further, variance in the “sizes” ofeach skeletal region, extracted as GMs of class variables,is not different, suggesting canal “shape” may be highlyvariable within populations. Variation in the canal andnoncanal aspects of the pelvis appears to be correlated infemales but not males, whereas variation in the limbs isindependent from that of the pelvis in both sexes. The pel-vis, therefore, appears to be relatively flexiblemorphologically.

ACKNOWLEDGMENTS

The author thanks the curators who provided access totheir collections: Lita Webley and Johan Binneman(Albany Museum, Grahamstown), James Brink (Florisbad



Research Station, National Museum, Bloemfontein), AlanMorris (University of Cape Town), Graham Avery (IzikoMuseums of Cape Town), Niles Lynnerup (University ofCopenhagen), Marta Mirazon Lahr and Mercedes Oku-mura (Duckworth Laboratory, University of Cambridge),Marie Besse and Genevieve Perreard (University ofGeneva), Patrick Semal (Institut Royal des SciencesNaturelles de Belgique), Monica Zavattaro and Silvia Boc-cone (Museo di Antropologia e Etnologia, Universita degliStudi di Firenze), Giorgio Manzi (Museo di Antropologia,Universita’ di Roma), Philippe Mennecier (Musee del’Homme), Jerome Cybulski (Canadian Museum of Civili-zation), and Ian Tattersall and Gisselle Garcia (AmericanMuseum of Natural History). The author is grateful toJay Stock for insightful discussions and to Peter Ellisonand two reviewers for comments that have significantlyimproved this article.

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Skeletal variability in the pelvis and limb skeleton of humans: Does stabilizing selection limit female pelvic variation?