Pelvic dimorphism in relation to body size and body size dimorphism in humans

Journal of Human Evolution 61 (2011) 631e643

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Pelvic dimorphism in relation to body size and body size dimorphism in humans Helen K. Kurki Department of Anthropology, University of Victoria, P.O. Box 3050 STN CSC, Victoria, BC V8W 3P5, Canada

a r t i c l e i n f o

a b s t r a c t

Article history: Received 24 August 2010 Accepted 31 July 2011

Many mammalian species display sexual dimorphism in the pelvis, where females possess larger dimensions of the obstetric (pelvic) canal than males. This is contrary to the general pattern of body size dimorphism, where males are larger than females. Pelvic dimorphism is often attributed to selection relating to parturition, or as a developmental consequence of secondary sexual differentiation (different allometric growth trajectories of each sex). Among anthropoid primates, species with higher body size dimorphism have higher pelvic dimorphism (in converse directions), which is consistent with an explanation of differential growth trajectories for pelvic dimorphism. This study investigates whether the pattern holds intraspecifically in humans by asking: Do human populations with high body size dimorphism also display high pelvic dimorphism? Previous research demonstrated that in some smallbodied populations, relative pelvic canal size can be larger than in large-bodied populations, while others have suggested that larger-bodied human populations display greater body size dimorphism. Eleven human skeletal samples (total N: male ¼ 229, female ¼ 208) were utilized, representing a range of body sizes and geographical regions. Skeletal measurements of the pelvis and femur were collected and indices of sexual dimorphism for the pelvis and femur were calculated for each sample [ln(M/F)]. Linear regression was used to examine the relationships between indices of pelvic and femoral size dimorphism, and between pelvic dimorphism and female femoral size. Contrary to expectations, the results suggest that pelvic dimorphism in humans is generally not correlated with body size dimorphism or female body size. These results indicate that divergent patterns of dimorphism exist for the pelvis and body size in humans. Implications for the evaluation of the evolution of pelvic dimorphism and rotational childbirth in Homo are considered. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: Obstetric selection Pelvis Sexual dimorphism

Introduction In mammals, the general pattern of body size dimorphism (often termed sexual size dimorphism, or SSD) is that males are larger than females, which is typically attributed to sexual selection promoting larger male body size (Abouheif and Fairbairn, 1997; Fairbairn, 1997; Badyaev, 2002). In contrast, many species display sexual dimorphism in the pelvis, with females exhibiting larger dimensions of the obstetric (pelvic) canal than males. Pelvic dimorphism has been attributed to selection relating to parturition (Schultz, 1949; Leutenegger, 1974; Leutenegger and Larson, 1985; Wood and Chamberlain, 1986; Ridley, 1995) or as a result of differential allometric growth trajectories between the sexes resulting from different hormonal milieus beginning at puberty (Schultz, 1949; Leutenegger, 1974; Tague, 2005), though these hypotheses are not mutually exclusive. The unique rotational childbirth mechanism of humans most certainly plays a role in

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determining the human patterns of pelvic dimorphism, thus the processes leading to pelvic dimorphism are of interest in examining the hominin fossil record and the evolutionary origins of human childbirth (Rosenberg, 1992; Ruff, 1995; Rosenberg and Trevathan, 2002). Male-dominated sexual dimorphism (males > females) in body size is common among mammal and bird species, while ectotherms typically show female-dominated body size dimorphism (Fairbairn, 1997, 2005; Blanckenhorn et al., 2007). Given the high prevalence of sexual size dimorphism in animals, it has long been a topic of intensive study. Rensch (1960) noted that in species where males are the larger sex, SSD tends to increase in magnitude with body size, such that larger-bodied species show greater magnitude of SSD. This pattern has been called Rensch’s Rule (Abouheif and Fairbairn, 1997; Fairbairn, 1997), and has become a major focus of studies of sexual dimorphism. Differences in the reproductive strategies of males and females lead to differential selection acting on each sex, and ultimately to the development of sexual dimorphism (Badyaev, 2002), and dimorphism in fossil species can therefore provide information about social behavior in extinct

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species (Plavcan, 2002). As such, for paleoanthropologists, the study of sexual dimorphism in primates takes on a particular importance. Primates, including humans, also fit the pattern of increasing sexual size dimorphism with increasing body size (Leutenegger, 1978; Leutenegger and Cheverud, 1982; Wolfe and Gray, 1982; Smith and Cheverud, 2002; although see Lindenfors and Tullberg, 1998; Gustafsson and Lindenfors, 2004). The intense focus on correlates of SSD has tended to distract attention away from examination of patterns of dimorphism of specific body regions (Schutz et al., 2009b). Sexual dimorphism in the pelvis has been shown in various mammal species; for example, sheep (Cloete et al., 1998), cattle (Johnson et al., 1988), mice and rats (Berdnikovs et al., 2007; Schutz et al., 2009a), grey fox (Schutz et al., 2009b), and many haplorhine primate species including humans (e.g., Leutenegger, 1974; Mobb and Wood, 1977; Steudel, 1981; Leutenegger and Larson, 1985; Tague, 1992, 1995; Kurki, 2007; St. Clair, 2007) display sexual dimorphism in the size of specific pelvic dimensions or aspects of pelvic shape. Females of these species tend to be larger than males for dimensions of the pelvic (obstetric) canal. Washburn (1948) established the ischiopubic index, a measure of the relative length of the pubis, as a useful indicator of sex from skeletal remains of primates. Studies investigating pelvic dimorphism in humans have found that some aspects follow the pattern of body size dimorphism (males > females) including dimensions of the hip bone (except pubic length), bi-iliac breadth, canal depth, and sacral length, while others show inverse dimorphism (females > males) including dimensions of the pelvic canal, bi-acetabular breadth, and public bone length (Tague, 1992; Arsuaga and Carretero, 1994; Kurki, 2005, 2007). As most of the pelvic dimensions that are larger in females than in males are related specifically to the obstetric canal, selection acting to enlarge the pelvic canal for parturition (obstetric selection) likely acts to generate this pattern, at least in part. Ridley (1995) demonstrated that in primates, the magnitude of pelvic dimorphism is related to neonatal brain size, which supports the obstetric selection hypothesis. Not all species, including many primates (e.g., Trevathan and Rosenberg, 2000; Tague, 2005), that exhibit pelvic dimorphism have large neonates relative to maternal size; therefore obstetric selection is not necessarily high for these species. Tague (2005) has suggested that Schultz’s hypothesis relating pelvic dimorphism to the development of secondary sexual characteristics (different allometric trajectories of growth between the sexes) is also a viable explanation. Using data from twelve anthropoid primate species, including Homo sapiens, Tague (2005) argued that primate species with higher body size dimorphism have higher pelvic dimorphism (in converse directions) due to sensitivity to testosterone, rather than specifically (or solely) to obstetric requirements. Tague does not consider the relationship between body size and dimorphism, but as some primates have been found to conform to this pattern, this implies that largerbodied primates should also display greater body size and pelvic dimorphism. While interspecific patterns of dimorphism need not have direct implications for intraspecific patterns of dimorphism, an examination of intraspecific patterns of pelvic and body size dimorphism may offer insights into how selective forces might work in generating morphological differences and aid in assessing the hypothesis that pelvic dimorphism results as a developmental consequence of secondary sexual differentiation within species. If hormone sensitivity is what generates high dimorphism in body size and pelvic size for a species, and if there are within-species, between-population differences in body size dimorphism, then one should expect similar effects on pelvic dimorphism under this hypothesis. Given a species such as humans, that display variation in body size parameters and levels of sexual dimorphism among

populations (e.g., Wolfe and Gray, 1982; Holden and Mace, 1999; Gustafsson and Lindenfors, 2004 [and references therein], 2009), one might expect that a similar relationship between body size, body size dimorphism and pelvic dimorphism exists within the species, to what Tague has shown for across primate species. This study investigates whether or not these patterns are consistent within H. sapiens by examining the relationships of body size and body size dimorphism to pelvic dimorphism across human populations, using skeletal indicators of pelvic size and body size. Unfortunately, such population-level data for other primate species are generally lacking in the literature, meaning that studies of variation in sexual dimorphism (body size, craniofacial, pelvic, etc.) in primates take an interspecific approach (e.g., Leigh and Shea, 1995; Tague, 1995, 2005; Smith and Leigh, 1998; Smith and Cheverud, 2002; Plavcan, 2002, 2003). Despite their large body size, humans show only moderate levels of body size dimorphism compared to many other primates (Plavcan and van Schaik, 1997; Tague, 2005). Pelvic and body size sexual dimorphism An examination of the factors that may play a role in the development of overall body size, and body size and pelvic dimorphisms, is central to investigating whether these dimorphisms are related, as would be expected for the secondary sexual characteristic (allometric trajectories) hypothesis, or independent, which would be consistent instead with the obstetric selection hypothesis. Several studies have examined these factors in primate and non-primate mammals, though few studies have included humans. Growth and development are regulated by a series of hormones that are secreted at particular times and in particular dosages over the course of ontogeny, and which are sex- and species-specific (see review in Bernstein et al., 2007). In an attempt to understand the role of hormones in the evolution of size differences among species, Bernstein et al. (2007) examine the levels of various hormones (insulin-like growth factor-I [IGF-I], insulin-like growth factor binding protein-3 [IGFBP-3], growth hormone binding protein [GHBP], dehydroepiandrosterone sulfate [DHEAS], testosterone, estradiol) in relation to body size in papionin primates, during ontogeny and in adults. Their results indicate that in interspecific comparisons, levels of IGH-I, estradiol and testosterone are not related to size differences across papionins, though levels of GHBP and DHEAS are correlated with body size, suggesting they play a role in interspecific size differences. In a later study, Bernstein et al. (2008) found that baboons and mangabeys differ in their circulating hormone levels and growth profiles across ontogeny, and in the relationships between hormone levels and withinspecies body size. These studies imply that there is not a single hormone-related mechanism for the development of body size differences across primate species, and that species-specific hormone-influenced growth patterns relate to within-species differences in body size. One implication of these findings and those of Berdnikovs et al. (2007) (see below) is that there may also be species-specific mechanisms for the development of body size and pelvic dimorphisms, as skeletal growth in males and females respond differently to circulating hormone levels. Body size dimorphism can result from different processes, namely different timing of growth cessation (bimaturatism) and different rates of growth between the sexes (see Badyaev, 2002 for detailed discussion). Leigh (1992) and Leigh and Shea (1995) demonstrate that across primate species different combinations of these two processes contribute to the development of SSD in difference species. Leigh (1992) found that there was no consistent pattern to the relative contribution of bimaturation versus

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differential growth rates in relation to body, while Leigh and Shea (1995) show that for hominoids there are significant differences in how these two processes contributed to SSD, even within the genus Pan. They conclude that these different patterns are related to differences in feeding ecology among the hominoid species. Together, these studies suggest that species-specific ontological processes result in both adult body size and sexual size dimorphism. While few studies of intraspecific sexual dimorphism have been conducted for primate species, other mammal studies have demonstrated that there are sex-specific responses to hormones related to skeletal growth, which result in sexual dimorphism in body size and pelvic size. Berdnikovs et al. (2007) test the allometric trajectories hypotheses for pelvic dimorphism by examining growth patterns in male and female laboratory rats (Rattus norvegicus). Since the studies of Bernstein and Crelin (1967) and Uesugi et al. (1992), the predominant view has been that the female morphology of the pelvis is the default shape and the male pelvic shape develops under the influence of androgens, beginning at puberty. However, more recent studies have suggested that androgens actually play a minimal role in promoting the pubertal growth spurt and skeletal maturation (Grumbach, 2000). Instead, the role of estrogen in the pubertal growth spurt and skeletal development is increasingly recognized, indicating that sexspecific timing of the effects of estrogen on skeletal growth may play a significant role in the development of skeletal dimorphisms (Grumbach, 2000). In their study of rat pelvic growth, Berdnikovs et al. (2007) found that dimorphism in shape was decoupled from size dimorphism such that while size differences appeared in later stages of growth (post-puberty), shape differences between the sexes appeared as early as their age group 1 (22e24 days), before the onset of puberty (age group 3). The authors “found the appearance of dimorphism to be a reflection of the complex combination of initial sex differences followed by dissimilarities in rates and directions of shape change between the sexes” (Berdnikovs et al., 2007:20). Up to the onset of puberty, the female pelvis may be considered the “default” shape, but after the onset of puberty, sexspecific responses to estrogen result in changes to the female growth trajectory while the male growth trajectory continues to follow the pattern of shape change established in earlier periods. As an alternative to the “female default” model of pelvic development, Berdnikovs et al. (2007) argue that sex-specific responses to estrogen, either through differences in estrogen concentration or the distribution of estrogen receptors on regions of the pelvic bones, lead to pelvic dimorphism rather than as part of global differences in skeletal growth between males and females. Androgens are constant throughout ontogeny, rather than contributing to a pubertal growth spurt in shape change in the male pelvis. The results of this study are counter to the hypothesis put forward by Tague (2005) that pelvic dimorphism is the result of general sensitivity to testosterone manifesting as high body size and pelvic dimorphism, and may provide clues to the mechanism through which obstetric selection may act to produce femalespecific pelvic morphology. Schutz et al. (2009a) examine the hypothesis that obstetric function is a critical determinant of pelvic dimorphism in their study of the effects of pregnancy status (nulliparous or parous) and litter size on pelvic size and shape in laboratory bred mice (Mus musculus domesticus). In mammals, significant changes to the hip bone occur during pregnancy (Todd, 1923; Kelley, 1979; Johnson et al., 1988; Tague, 1988, 1990; Cox and Scott, 1992), which may further enhance pelvic dimorphism, for example, Specker and Binkley (2005) found that high parity in humans is related to increased bone size (femoral neck bone area and cross-sectional

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area of the radius). In their study of mice, Schutz et al. (2009a) found significant differences in the structure of the hip bone of parous relative to nulliparous females. In overall body length, parous females and male mice, were longer than nulliparous females, suggesting that parity events affect the size of skeletal elements in a systematic manner, including the pelvis. Overall size of the hip bone was also largest in the parous females, followed by the nulliparous females; males were smallest. Significant shape differences were found between parous and nulliparous females. Further, Schutz and colleagues suggest the shape changes to the hip bone of the parous females are consistent with other mammalian studies, including humans, which indicate a “consistent pattern of pelvic ‘adjustment’ localized at the pelvic midplane (the most constricted region)” (Schutz et al., 2009a:841). These results support the role of obstetric function in generating pelvic sexual dimorphism. Sexual dimorphism in strepsirrhine primates is less studied than that of haplorhine primates, though they form an excellent contrast since they show low or no sexual dimorphism in body size (Kappeler, 1991; Smith and Jungers, 1997), cranial size (Jenkins and Albrecht, 1991), and pelvic size (Leutenegger, 1973). Strepsirrhines also tend to have smaller neonates, relative to maternal size, than haplorhine primates (St. Clair, 2007). As a test of the obstetric selection hypothesis, St. Clair (2007) examined sexual dimorphism in Microcebus, the smallest extant primate genus. Her results show that while males and females do not differ in femoral size, females are larger than males for several pelvic dimensions (sacral width, pelvic height, pubic length, and pubis-ischial tuberosity and pubissacral lengths). An obstetric selection explanation for the pelvic dimorphism, rather than as a correlate of skeletal size dimorphism, is supported by the presence of pelvic dimorphism in the absence of skeletal size dimorphism. Finally, as the secondary sexual character hypothesis posits a relationship between two aspects of dimorphism, that of body size and of pelvic size, the relationships among dimorphisms in various aspects of the body are relevant to the testing of this hypothesis. However, few studies have specifically examined these relationships. In an examination of size and shape dimorphism in two species of grey fox (Urocyon littoralis and U. cinereoargenteus), Schutz et al. (2009b) noted different patterns of cranial versus pelvic dimorphism in these two species. Neither species shows significant dimorphism in size or shape of the cranium, and though both species display sexual dimorphism in size (centroid size) of the hip bone, only the smaller-bodied species, U. littoralis, exhibits significant shape dimorphism. Schutz and colleagues suggest that factors such as offspring size and locomotor mode (e.g., for canids, degree of cursoriality) play a more important role in sexual dimorphism in the pelvis than overall allometric effects of total body growth. They conclude that “it may not be appropriate to expect that dimorphism patterns are uniform throughout an organism and parallel those that we see for body size” (Schutz et al., 2009b:351). This conclusion is consistent with the varying patterns of craniofacial dimorphism in relation to body size dimorphism that Plavcan (2003) found across primate taxa. Together these studies imply that sexual dimorphism in different aspects of a species’ anatomy may vary significantly, including pelvic in relation to body size dimorphism, and therefore the mechanisms producing dimorphism are likely complex. Further, it appears from the results of the studies discussed above that there are species-specific and sex-specific responses to growth-related hormones, leading to species- and sex-specific growth patterns generating body size dimorphism. The notion of body and pelvic dimorphisms being related to the same process, secondary sexual differentiation via a general sensitivity to growth-related hormones (e.g., testosterone) is therefore called

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into question. This study attempts to contribute to the elucidation of patterns and relationships of body size and pelvic sexual dimorphisms by looking specifically at variation among human populations. If secondary sexual differentiation is the mechanism by which these dimorphisms are produced, rather than obstetric selection acting specifically on the female pelvis (and some other selection factor, such as sexual selection acting on male relative to female body size), then one would expect a positive relationship between body size and pelvic dimorphisms within humans, as Tague (2005) has demonstrated across primate species. As Tague’s (2005) study examined interspecific dimorphism, it is important to note that the current study does not test the same hypothesis. Instead, this study’s analyses are focused on documenting patterns of, and testing hypotheses relating to, intraspecific dimorphism, which may offer insights into how selective forces might work to generate morphological differences and whether these forces lead to speciation or not.

estimated. Only skeletal material from adult individuals (i.e., with the epiphyses of the iliac crest and ischial tuberosity showing some fusion) were included. Sex was determined using commonly accepted non-metric pelvic characteristics (ventral arc, subpubic concavity, ischiopubic ramus ridge, subpubic angle, and greater sciatic notch width) and, when available, cranial characteristics (supraorbital margin, mastoid process, nuchal crest, prominence at glabella, and mental eminence) (Buikstra and Ubelaker, 1994). Where there are both male and female features present on an individual skeleton, the preponderance of data indicating male or female was taken in the assignment of sex to the specimen. Meindl et al. (1985) have reported error rates in sex assessment of 6.8% when using only pelvic features and 3% when using both pelvic and cranial features. Measurements were taken of the hip bone, articulated pelvis, and femur (Fig. 1 and Table 2). The measurements of the articulated pelvis quantify the overall width of the pelvis (bi-actetabular breadth) as well as antero-posterior, medio-lateral, and posterior space dimensions of the three planes of the pelvic canal (inlet, midplane, and outlet). For the articulated pelvic measurements, the right and left hip bones and sacrum were articulated anatomically and bound together firmly with adhesive tape and elastic bands. This prevented the bones from shifting during measurement. No accommodations were made for the cartilage components of the pubic symphysis and sacroiliac joints that would have been present in the living person. The geometric mean of femoral length and head diameter was used as a proxy for body size (hereafter referred to as femoral size), as this serves to include aspects of both stature (femoral length) and body mass (femoral head diameter). Body mass can be estimated from formulas using the femoral head (Ruff et al., 1991; McHenry, 1992), or stature (estimated from femoral length) and bi-iliac breadth (Ruff, 1994; Ruff et al., 2005), and these body mass estimates could be used instead of femoral size to remain consistent with most studies of sexual dimorphism that use body mass. However, for the purposes of the present study the use

Materials and methods The relationships among pelvic dimorphism, body size and body size dimorphism in human populations are examined using eleven skeletal samples (total N: males ¼ 229, females ¼ 208) (Table 1). Kurki (2007) demonstrated that in some small-bodied human populations, relative pelvic canal size can be larger than in largebodied human populations, and as noted above, larger-bodied human populations display greater body size dimorphism than smaller-bodied populations (Wolfe and Gray, 1982; although see; Gustafsson and Lindenfors, 2004). Climate has also been implicated as a factor contributing to human size dimorphism (Gustafsson and Lindenfors, 2009). Human skeletal samples representing populations of varying body sizes and proportions and from diverse geographical regions are therefore included in this study. Since most of the samples are archaeological in origin, attributes of the individual specimens such as age at death and sex had to be

Table 1 Details of skeletal samples included in this study. Sample

Date

African Pygmy

20th C.

Philippines

19th C.

Andaman Islands

ca. 1860e1900

Femoral Length (mm)

14

South Africa

240e5370 BP (C )

Tierra del Fuego

ca. 1880

Portugal

19th-early 20th C.

Australia

19th C.

North Africa

2000 BC e AD 550

EuropeaneAmerican

19th-early 20th C

Inuit

AD 800e1900

Denmark

Medieval

a

Female Male Female Male Female Male Female Male Female Male Female Male Female Male Female Male Female Male Female Male Female Male

Institutionb

Femoral Head Diameter (mm)

Mean

S.D.

N

ISDa

Mean

S.D.

N

ISDa

362.6 383.9 372.2 404.1 380.9 388.3 400.8 409.3 388.0 417.0 400.5 441.8 429.3 449.5 414.1 442.2 418.2 445.7 406.5 432.3 423.8 470.2

14.9 32.5 13.5 23.5 12.8 30.5 24.5 28.5 12.3 19.0 19.4 18.2 10.1 21.6 18.9 30.8 26.3 22.7 24.6 19.2 27.7 20.9

6 7 7 8 8 5 24 28 8 9 40 40 5 9 21 28 40 40 27 33 10 9

0.057

35.2 38.6 36.5 40.5 36.5 38.8 37.0 40.2 40.9 45.4 40.3 46.3 38.0 43.2 39.7 44.8 42.0 47.5 44.0 48.5 43.0 49.4

1.2 1.9 1.4 3.1 2.6 2.8 2.0 2.6 1.8 3.1 2.3 2.3 1.9 2.0 1.8 2.9 2.2 2.7 1.9 1.9 2.3 2.7

6 7 7 8 7 6 24 27 7 9 40 40 5 9 21 27 40 40 27 32 10 9

0.091

IRSN, MdH, UG

0.105

MdH

0.061

AMNH, DC, NHM

0.083

ALM, IMCT, NMB, UCT

0.103

MAE, MdH, UR

0.139

MAUC

0.128 0.120

AMNH, DC, MAE, MdH, NHM, UG AMHN, DC, UCOP

0.123

CMNH

0.099

AMNH, CMC

0.139

UCOP

0.082 0.019 0.021 0.072 0.098 0.046 0.066 0.064 0.061 0.104

Index of Sexual Dimorphism (ISD) ¼ ln(male/female). ALM, Albany Museum; AMNH, American Museum of Natural History; CMC, Canadian Museum of Civilization; CMHN, Cleveland Museum of natural History; MdH, Musee de l’Homme; DC, Duckworth Collection; IMCT, Iziko Museums of Cape Town; IRSN, Institut Royal des Sciences Naturelles de Belgique; MAUC, Museu Antropologica, University of Coimbra; MAE, Museo di Antropologia e Etnologia, Università degli Studi di Firenze; NHM, Natural History Museum; NMB, National Museum, Bloemfontein; UCOP, University of Copenhagen; UCT, University of Cape Town; UG, University of Geneva; UR, Museo di Antropologia, Universita’ di Roma. b

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Figure 1. Measurements of the pelvis and hip bone (see Table 2 for descriptions): a) anterior view of pelvis; b) posterior view of pelvis; c) and d) medial view of right hip bone with sacrum; e) lateral view of right hip bone. A: bi-acetabular breadth; B: inlet A-P; C: inlet M-L; D: inlet posterior; E: midplane A-P; F: midplane M-L; G: midplane posterior; H: outlet A-P; I: outlet M-L; J: outlet posterior; K: hip bone length; L: ischial length; M: pubic length.

of femoral size avoids adding additional error to body size dimorphism calculations among the samples. This follows from the findings of Kurki et al. (2010) that the reconstruction of body mass for samples at the low end of the human body mass range may be subject to large disagreements among methods, and thus the reliability of estimates may be questioned. Table 2 Descriptions of measurementsa used in this study (see also Fig. 1). Variable Femoral length Femoral head diameter Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length

Description Maximum length of the femur Maximum diameter of the femoral head Distance between acetabulae (Fig. 1, line A) Sacral promontory to dorsomedial superior pubis (B) Maximum distance between linea terminalis (C) Curved length of linea terminalis from inlet M-L to apex of auricular surface (D) From junction of 4th and 5th sacral vertebrae to dorsomedial inferior pubis (E) Between ischial spines (F) S4-S5 junction to ischial spine (G) Apex of fifth sacral vertebrae to dorsomedial inferior pubis (H) Distance between inner margins of transverse ridge of ischial tuberosities (I) Apex of S5 to ischial tuberosity (J) From most superior point on iliac crest to most inferior point of ischial tuberosity (K) Distance from Schultz’s point Ab to transverse ridge of ischial tuberosity (L) Distance from Schultz’s point A to superior aspect of symphyseal face (M)

a Measurement definitions are from Tague (1989), Berge et al. (1984), Berge (1998), and Buikstra and Ubelaker (1994). b Schultz’s Point A is at the intersection in acetabulum of the three elements of the hip bone, characterized by a notch and irregular bone.

Statistical design Sex-specific mean values were used to calculate indices of sexual dimorphism (ISD) for each measurement as ln(male/female). Smith (1999) carefully examines various methods of quantifying dimorphism using ratios and residuals from regression analysis, including the potential pitfalls of applying these dimorphism calculations in statistical analyses. It is important to note that when using ratios such as ln(male/female), the choice of which sex is in the numerator and which in the denominator will influence the resultant value, therefore indices should be interpreted with caution. Dimorphism in body size (femoral size) and hip bone size (males > females) tend to be in the converse direction to pelvic canal dimorphism (females > males). Using this formula for the indices, positive index values indicate the male mean is larger than the female mean, and negative values indicate the female mean is larger. Samples sizes for ISD calculations vary as a result of completeness of skeletons, but not all skeletons preserve the required skeletal elements or anatomical points for all of the measurements. Sexual dimorphism was also investigated within each skeletal sample using t-tests and Wilcoxon tests (smaller samples: Andaman Islands, Philippine, African Pygmy, Australian, Denmark, Terra del Fuego) for significant differences between female and male mean values for each variable. Correlation and linear regression were used to characterize the relationships among variables and to test for deviation from isometry in these relationships. The following regression analyses were conducted: 1) pelvic dimorphism (PSD) vs. femoral size dimorphism (FSD) to examine the relationships between pelvic and body size dimorphism; and 2) PSD vs. female femoral size to examine the relationship of pelvic dimorphism to body size. Following Smith (Smith, 1999, 2009; Smith and Cheverud, 2002) and Plavcan (2003), the reduced major axis model (model II) was used to regress PSD on FSD, and

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the least squares model (model I) was used in the regression of PSD on female femoral size (ln-transformed). As debate continues in the sexual dimorphism literature on the use of model I and II regression (for discussion of this issue see Smith, 1999, 2009), least squares (model I) regression statistics are also provided for PSD on FSD. Deviations from the condition of isometry in the relationships between pelvic dimorphism and femoral dimorphism and femoral size are indicated by regression slopes which are significantly different from 1.0 (using ln-transformed data), based on an examination of 95% confidence intervals of the slope: a slope greater than 1.0 indicates positive allometry and a slope less than 1.0 indicates negative allometry between the variables (Jungers et al., 1995; Smith and Cheverud, 2002; Smith, 2009). Pearson’s and Spearman’s correlation coefficients were calculated, and although none of the indices of sexual dimorphism (one value for each sample, N ¼ 11) distributions deviated from normality (KolmorgorveSmirnov, AndersoneDarling, and Cramer von Mises tests, results not shown), the sample size warrants consideration of the nonparametric correlation. If pelvic dimorphism in humans follows a similar pattern to that demonstrated by Tague (2005) across anthropoid primate species, then significant relationships between the level of femoral size dimorphism and the level of pelvic dimorphism should be found in these analyses. The direction of this relationship will however vary depending on which variables are being considered. Since pelvic canal dimorphism is females > males, the indices are negative values, while for femoral size dimorphism males > females, the indices are positive values. In this case a negative correlation and regression slope would indicate that PSD increases (moves away from a zero value) with an increase in FSD. In contrast, for cases where males > females for the pelvic and femoral variables, a positive correlation and regression slope would indicate increasing PSD with FSD. A similar consideration applies to the evaluation of PSD with femoral size. RMA analyses were performed using PAST version 2.02 (Hammer et al., 2001), and t-tests, Wilcoxon tests and least squares regressions using SAS version 9.1. Two levels of statistical significance were considered in the evaluation of the results to account for the multiple comparisons in this study:  a Dunn-Sidák conservative alpha value [a0 ¼ 1  (1  a)1/k, where a ¼ 0.05 and k ¼ the number of comparisons] (Sokal and Rohlf, 1995), and the less conservative p  0.01. This less conservative alpha was considered as small samples sizes for several skeletal samples may influence the pattern of statistical significance. Results The variation in the relationship between female body mass and female stature (represented by femoral head diameter and femoral length, respectively) among the samples is clear in the sample descriptive statistics (Table 1). Samples vary in body proportions; for example, some are short with low body mass (e.g., Andaman Islanders, African Pygmies, Philippine and southern Africans), others are short with larger body mass (e.g., Fuegians and Portuguese), tall with lower body mass (e.g., Australians and North Africans), or tall with larger body mass (e.g., EuropeaneAmericans, Inuit and Danes). The indices of sexual dimorphism (ISD) and the ttest and Wilcoxon statistics for the pelvic and femoral size variables for each sample are provided in Table 3. The results of the t-tests and Wilcoxon tests illustrate that the statistical significance of sexual dimorphism varies among the samples. Variation in sample size likely plays a role in the findings of patterns of statistical significance (or lack thereof), particularly at the conservative alpha value (p  0.004 with 14 variables examined for each sample). For the six samples for which the Wilcoxon test was applied, most variables are not significantly different between

females and males at the conservative alpha. For example, the African Pygmy sample displays no significant differences between females and males at this alpha, though at a less conservative alpha of 0.01, several pelvic canal dimensions (inlet posterior, midplane A-P, M-L, and posterior, and outlet A-P) and ischial length are dimorphic. Similar results are found for the Philippine, Andaman Island, Australian and Denmark samples, where it is largely the biacetabular breadth, outlet and midplane (medio-lateral and posterior spaces) and hip bone and ischial lengths that are significant at the less conservative alpha. Females are always the larger sex for the bi-acetabular and pelvic dimensions, and males are the larger sex for the latter two variables. The Fuegians display a different pattern with most variables reaching statistical significance, even at the conservative alpha. Femoral size is significantly different only in the Danes and Australians (males > females) at the conservative alpha. The rest of the samples, with larger sample sizes (southern Africa, Portugal, Northern Africa, EuropeaneAmerican, and Inuit) display more consistent patterns of significant sexual dimorphism in the t-test results (Table 3). All are significantly different (males > females) for femoral size, and medio-lateral breadths and posterior spaces of the canal planes (females > males), at the conservative alpha. The remaining variables are not statistically significant in at least one sample. All dimensions are significant for the EuropeaneAmerican sample. Although it is apparent that patterns of statistical significance in dimorphism among the samples are complex, the indices of sexual dimorphism (Table 3) provide a means for the comparison of levels of dimorphism among these varied samples, and the examination of relationships between pelvic dimorphism and femoral size and dimorphism. Females are larger than males [negative values for ln(male/female)] for the dimensions of the planes of the pelvic canal (A-P, M-L, and posterior spaces of the inlet, midplane and outlet), bi-acetabular breadth, and pubic bone length, although most of these differences do not reach statistical significance. For the rest of the variables, which reflect hip bone size and body size, males are larger than females (again, with a few exceptions where females > males, though with low ISD values). The patterns of the magnitude of pelvic and femoral dimorphism across the samples are complex, yet the magnitude of dimorphism in the pelvic canal is larger than that of measures of the hip bone or femur. The results of the regression of PSD on FSD are given in Table 4. In the majority of cases, the correlations between pelvic and femoral size dimorphism are not significant; only inlet M-L (Pearson’s ¼ 0.802, p ¼ 0.003; Spearman’s ¼ 0.573, p ¼ 0.066) and hip bone length (Pearson’s ¼ 0.780, p ¼ 0.005; Spearman’s ¼ 0.791, p ¼ 0.004) are significant at the conservative alpha (p  0.004 for 13 comparisons). Note that in both cases only the parametric or nonparametric test is significant. The RMA regression slopes for these two variables indicate isometric relationships, although the least squares regression slope for hip bone length suggests a negative allometric relationship. Bivariate graphs for these variables (Fig. 2a and b) illustrate the distribution of the sample ISDs. As inlet M-L are negative indices (females > males) and FSD are positive indices (males > females), for inlet M-L the positive correlation and regression slope indicate that the samples with lower FSD have higher levels (negative indices farther from zero) of inlet M-L dimorphism. The opposite is the case for hip bone length, which has all positive indices, therefore the positive correlation and slope indicate samples with low FSD have low hip bone length dimorphism relative to samples with high FSD. Table 5 provides the results of the regression of pelvic and femoral dimorphism on female femoral size [ln(femoral size)]. These results illustrate that pelvic and femoral dimorphisms are not related to female size (femoral size). At the conservative alpha

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Table 3 Descriptive statistics (in mm) and indices of sexual dimorphisma for pelvic and femoral variables by sample. Variable

African Pygmy Female

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

S.D.

N

Mean

S.D.

N

90.59 102.33 108.83 33.25 114.83 83.33 62.67 112.83 88.30 77.42 168.58 64.17 65.99 112.97

3.52 6.71 7.83 3.45 6.97 3.30 3.34 9.33 6.27 6.37 5.73 2.94 2.82 2.83

6 6 6 6 6 6 6 6 6 6 6 6 6 6

88.83 95.50 103.17 25.33 99.17 76.64 52.83 95.50 79.50 66.08 175.71 71.41 62.73 121.65

3.91 5.68 6.59 3.14 5.12 3.44 3.60 5.17 4.88 7.03 9.20 3.90 5.17 7.65

6 6 6 6 6 6 6 6 6 6 7 7 7 7

0.695 0.099 0.326 0.005 0.010 0.010 0.005 0.010 0.040 0.015 0.319 0.008 0.532 0.013

Female

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

90.92 104.33 105.00 25.33 111.60 83.65 61.33 107.80 105.99 79.10 166.85 63.98 63.72 117.66

3.66 6.44 4.69 4.06 6.02 6.01 4.54 10.38 9.55 5.12 6.43 3.01 4.37 4.93

6 6 6 6 5 3 3 5 5 5 10 10 10 7

76.11 94.71 89.33 21.33 100.71 63.18 47.25 98.83 73.10 61.75 176.79 68.04 61.34 121.32

7.15 5.25 9.24 4.33 5.59 6.87 3.05 4.83 7.70 2.54 10.08 5.30 7.13 7.29

6 7 6 6 7 5 6 6 6 6 7 7 7 5

Mean

S.D.

N

Mean

S.D.

N

98.69 99.38 114.00 28.13 114.88 88.69 62.75 110.38 101.84 77.31 169.75 68.83 72.38 116.47

5.63 6.25 6.07 3.97 9.20 5.42 5.79 10.81 8.23 8.66 7.85 4.32 3.82 2.76

8 8 8 8 8 6 6 8 8 8 8 8 8 7

89.17 91.25 101.38 22.19 98.38 73.73 47.80 94.75 84.07 58.38 180.31 71.91 66.66 127.90

7.42 4.68 9.18 2.48 3.50 5.09 2.59 3.45 10.45 4.16 16.37 5.92 5.68 7.85

8 8 8 8 8 4 5 8 8 8 8 8 8 8

0.178 0.097 0.162 0.172 0.103 0.281 0.261 0.087 0.372 0.248 0.058 0.062 0.038 0.031

p-valuec

0.002 0.072 0.007 0.141 0.013 0.036 0.024 0.063 0.003 0.002 0.045 0.103 0.602 0.541

Female

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

113.18 106.00 129.78 31.89 134.67 108.53 76.43 129.44 118.97 94.78 192.78 76.04 79.93 126.46

4.29 7.48 5.78 3.41 9.87 6.03 6.51 10.97 7.29 7.60 7.45 4.08 4.78 4.17

9 9 9 9 9 6 7 9 9 9 9 9 9 7

103.41 101.43 119.57 25.75 114.86 88.48 58.25 111.57 96.47 76.21 204.79 81.85 75.26 137.53

4.53 5.61 6.68 5.08 8.76 6.86 6.22 8.81 9.07 7.94 8.72 3.69 3.94 7.56

14 14 14 14 14 11 12 14 14 14 14 14 14 9

S.D.

N

Mean

S.D.

N

98.65 101.00 111.56 28.58 122.68 96.46 72.93 122.25 99.12 85.91 173.78 70.60 65.37 121.70

6.64 10.41 8.83 6.40 12.72 9.59 7.69 11.49 9.57 7.80 10.02 3.86 5.78 6.33

17 18 18 18 19 12 15 16 16 16 27 27 26 24

86.24 91.44 96.14 20.75 106.38 80.59 55.22 102.00 76.95 64.53 179.22 73.87 59.28 128.11

5.55 7.64 8.23 5.24 7.99 7.16 4.52 7.77 8.00 4.28 12.60 5.24 5.66 8.46

14 16 14 14 16 11 16 15 13 15 28 31 30 27

0.090 0.044 0.082 0.214 0.159 0.204 0.272 0.149 0.210 0.218 0.060 0.074 0.060 0.084

p-valuec

0.000 0.112 0.001 0.002 0.001 0.001 0.000 0.001 0.000 0.000 0.002 0.002 0.027 0.005

Female

Male

0.135 0.099 0.149 0.320 0.143 0.180 0.278 0.181 0.253 0.286 0.031 0.045 0.098 0.051

ISD

Mean

S.D.

N

Mean

S.D.

N

111.40 109.83 125.80 32.10 119.50 99.98 67.73 111.50 112.57 84.71 193.05 75.72 72.29 127.03

7.39 10.01 8.68 5.01 8.12 9.16 6.79 15.91 11.73 8.43 8.36 3.34 4.83 6.16

40 40 40 40 40 21 28 40 40 40 40 40 40 40

107.46 101.08 118.65 24.99 114.23 86.69 57.80 107.88 99.04 75.19 212.08 84.67 71.46 143.04

5.97 9.27 5.60 3.81 6.82 7.08 5.19 6.73 7.19 7.69 8.00 4.09 4.04 5.84

40 40 40 40 40 28 33 40 40 40 40 40 40 40

Australia Female

p-valuec

0.009 0.021 0.008 0.005 0.001 0.009 0.006 0.003 0.002 0.000 0.151 0.327 0.022 0.005

p-valuec

0.000 0.005 0.000 0.001 0.000 0.000 0.000 0.000 0.000 0.000 0.083 0.010 0.000 0.004

Portugal

Male

Variable

0.101 0.085 0.117 0.237 0.155 0.185 0.272 0.153 0.192 0.281 0.060 0.044 0.082 0.094

ISD

Mean

Terra del Fuego Female

ISD

Southern Africa

Male

Variable

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

0.020 0.069 0.053 0.272 0.147 0.084 0.171 0.167 0.105 0.158 0.041 0.107 0.051 0.074

p-valuec

Andaman Islands Female

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

ISD

Mean

Variable

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

Philippines

Male

0.036 0.083 0.059 0.250 0.045 0.143 0.159 0.033 0.128 0.119 0.094 0.112 0.011 0.119

p-valuec

0.011 0.000 0.002 0.000 0.002 0.000 0.000 0.190 0.000 0.000 0.000 0.000 0.410 0.000

Northern Africa

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

104.40 105.63 118.13 33.94 118.75 97.01 66.36 115.13 107.19 81.56 184.31 71.81 71.53 127.71

8.83 10.69 8.89 5.02 13.26 10.05 6.69 14.15 9.13 7.58 8.49 5.71 7.70 4.03

8 8 8 8 8 6 7 8 8 8 8 8 8 5

91.31 102.40 111.00 24.89 106.30 72.89 48.50 100.00 83.32 61.33 196.91 76.44 70.04 139.29

7.52 8.03 5.81 4.49 5.87 11.29 6.26 6.24 12.13 7.15 6.01 3.09 2.64 4.53

8 10 9 9 10 8 9 9 8 9 11 11 11 9

0.134 0.031 0.062 0.310 0.111 0.286 0.313 0.141 0.252 0.285 0.066 0.062 0.021 0.087

p-valuec

0.006 0.500 0.091 0.006 0.023 0.005 0.001 0.013 0.001 0.001 0.003 0.040 0.650 0.002

Female

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

107.72 110.81 122.41 34.17 119.33 99.15 68.00 112.11 115.79 82.81 187.08 73.60 74.44 128.25

5.58 8.73 7.53 4.50 8.21 6.70 8.71 9.74 9.23 7.64 6.70 3.53 5.72 5.00

17 21 17 21 21 10 12 18 17 18 20 21 21 21

99.03 98.43 113.96 26.15 110.33 80.26 53.26 103.27 91.81 67.00 201.04 79.66 70.54 140.73

6.53 8.26 7.22 3.99 7.41 6.54 3.96 7.13 9.66 7.06 8.07 4.46 3.81 8.24

23 28 24 24 27 17 17 26 23 26 28 27 27 27

p-valuec

0.084 0.000 0.118 0.000 0.072 0.001 0.268 0.000 0.078 0.000 0.211 0.000 0.244 0.000 0.082 0.001 0.232 0.000 0.212 0.000 0.072 0.000 0.079 0.000 0.054 0.011 0.093 0.000 (continued on next page)

638

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Table 3 (continued) Variable

EuropeaneAmerican Female

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

Inuit

Male

p-valuec

ISD

Mean

S.D.

N

Mean

S.D.

N

117.57 112.78 132.28 32.10 121.63 105.49 68.90 114.65 118.26 83.89 201.45 78.74 79.55 132.46

7.43 11.72 8.40 6.00 9.09 9.46 6.34 9.18 11.22 9.67 9.65 4.55 5.24 6.56

40 40 40 40 40 32 39 40 39 40 40 39 40 40

108.35 104.00 122.60 24.15 112.75 85.52 54.93 105.00 99.00 71.86 215.06 85.00 73.97 145.41

6.80 7.64 9.45 3.53 8.89 6.97 6.01 8.05 11.63 7.34 11.09 3.78 4.30 6.96

40 40 40 40 40 40 40 40 40 40 40 40 40 40

0.082 0.081 0.076 0.285 0.076 0.210 0.227 0.088 0.178 0.155 0.065 0.076 0.073 0.093

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

Variable

Female

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

115.56 104.52 130.70 30.69 127.44 110.89 75.05 120.56 116.88 90.28 204.09 80.24 82.59 133.66

5.85 9.45 8.19 4.11 12.59 7.27 7.10 13.35 9.66 10.92 14.79 5.48 5.26 6.59

27 27 27 27 27 9 10 27 27 27 27 27 27 27

105.68 99.42 119.64 24.36 120.09 91.91 63.10 114.39 96.21 80.00 217.23 88.28 77.17 144.79

7.94 7.28 7.11 3.93 7.63 6.31 5.16 7.32 11.25 8.35 7.42 4.45 5.27 4.53

32 33 33 33 33 18 21 33 31 33 33 33 33 32

0.089 0.050 0.088 0.231 0.059 0.188 0.174 0.052 0.195 0.121 0.062 0.095 0.068 0.080

p-valuec

0.000 0.022 0.000 0.000 0.011 0.000 0.000 0.038 0.000 0.000 0.000 0.000 0.000 0.000

Denmark Female

Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizeb

Male

ISD

Mean

S.D.

N

Mean

S.D.

N

121.21 103.30 133.00 28.44 120.30 103.75 67.63 111.33 122.04 84.22 203.15 80.20 83.03 134.90

4.16 10.32 6.91 3.66 5.70 6.38 8.44 7.98 8.94 10.85 10.06 3.97 4.89 6.31

8 10 8 8 10 3 4 9 7 9 10 10 10 10

111.55 101.33 126.63 24.25 117.63 89.22 58.79 110.38 101.69 75.06 223.17 88.75 77.16 152.40

7.29 12.36 10.58 4.16 9.05 5.71 1.60 10.20 9.04 4.43 5.97 3.61 3.89 7.07

8 9 8 8 8 7 7 8 8 8 9 9 9 9

0.083 0.019 0.049 0.159 0.022 0.151 0.140 0.009 0.182 0.115 0.094 0.101 0.073 0.122

p-valuec

0.007 0.655 0.184 0.036 0.553 0.017 0.162 0.952 0.000 0.041 0.000 0.001 0.016 0.000

a

Index of sexual dimorphism (ISD) ¼ ln (male/female). Femoral size is the geometric mean of femoral length and head diameter. Results of t-test or Wilcoxon tests (Monte Carlo p-value estimates for exact test) for significance of difference between female and male means. Bolded values are significant at a conservative Dunn-Sidak alpha value (p  0.004). Wilcoxon tests used for small samples (Andaman Islands, Australian, African Pygmy, Philippines, Denmark, Terra del Fuego). b c

(p  0.003 for 15 comparisons), none of the correlations are significant. At a less conservative alpha (p  0.01) midplane A-P is statistically significant (Pearson’s ¼ 0.734, p ¼ 0.010; Spearman’s ¼ 0.763, p ¼ 0.006), while outlet A-P reaches statistical

significance only for the Spearman’s coefficient (Pearson’s ¼ 0.671, p ¼ 0.024; Spearman’s ¼ 0.736, p ¼ 0.010). The regression lines indicate isometric relationships. For comparison, the regression of FSD on male femoral size is also included in Table 5. The

Table 4 Regressiona statistics (N ¼ 11) for comparisons of pelvic dimorphism and femoral size dimorphism. Variable ISD Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length a

Pearsonb

p-value

RMA slopec

S.E. slope

0.642 0.392 0.804 0.085 0.525 0.393 0.494 0.517 0.694 0.546 0.781 0.524 0.145

0.034 0.233 0.003 0.804 0.097 0.232 0.123 0.103 0.018 0.082 0.005 0.098 0.671

1.680 1.174 1.456 1.957 1.801 2.196 2.200 2.195 2.693 2.621 0.715 0.897 0.986

0.429 0.360 0.290 0.650 0.510 0.674 0.637 0.626 0.647 0.732 0.149 0.255 0.325

95% C.I.d 2.912; 2.242; 2.253; 3.917; 3.293; 4.198; 4.074; 4.028; 4.532; 4.756; 1.128; 1.644; 1.964;

0.969 0.615 0.941 0.978 0.985 1.149 1.188 1.196 1.600 1.444 0.453 0.489 0.495

Spearmane

p-value

OLS slopef

S.E. slope

95% C.I.

0.491 0.282 0.573 0.182 0.455 0.227 0.400 0.518 0.545 0.527 0.791 0.336 0.145

0.125 0.401 0.066 0.593 0.160 0.502 0.223 0.102 0.083 0.096 0.004 0.312 0.811

1.078 0.461 1.169 0.167 0.942 0.864 1.100 1.134 1.869 1.432 0.558 0.470 0.143

0.430 0.361 0.288 0.650 0.509 0.675 0.640 0.626 0.646 0.732 0.149 0.255 0.324

0.104; 2.052 0.356; 1.278 0.518; 1.820 1.305; 1.638 0.210; 2.094 0.662; 2.390 0.358; 2.538 0.282; 2.551 0.408; 3.330 0.224; 3.088 0.222; 0.894 0.106; 1.047 0.591; 0.876

Femoral size is the geometric mean of femoral length and head diameter. Pearson’s correlation coefficient (r), significant values at a conservative alpha (p  0.004) are indicated in bold. c Slope of the Reduced Major Axis (Model II) regression line. None of these slopes (for regressions with significant correlation coefficients at the conservative alpha) differ significantly from isometry (slope ¼ 1.0), as indicated by the 95% confidence intervals. d Asymmetric 95% confidence intervals of RMA slope calculated following Hofman (1988). e Spearman’s correlation coefficient, significant values at a conservative alpha (p  0.004) are indicated in bold. f Slope of the Least Squares (Model I) regression line. For regressions with significant correlation coefficients at the conservative alpha, only hip bone length indicates deviation from isometry (slope ¼ 1.0), as indicated by the 95% confidence intervals. b

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Discussion

Figure 2. Bivariate graphs of pelvic indices of dimorphism on femoral size indices dimorphism [ISD ¼ ln(male/female], with RMA (dashed) and OLS (solid) regression lines of best fit. OLS regression line includes 95% confidence intervals: a) inlet M-L ISD on femoral size ISD; b) hip bone length ISD on femoral size ISD.

correlation coefficients are higher (Pearson’s ¼ 0.762, p ¼ 0.006; Spearman’s ¼ 0.664, p ¼ 0.026) than between FSD and female femoral size (Pearson’s ¼ 0.543, p ¼ 0.084; Spearman’s ¼ 0.473, p ¼ 0.142), but not statistically significant at the highly conservative alpha. Fig. 3aec illustrates these relationships and the wide deviations from the line of regression found in these analyses. As with the interpretation of PSD on FSD, the meaning of the direction of the slope differs depending on the analysis. For midplane and outlet AP (Fig. 3a and b), which have negative indices for all samples, the positive correlation and regression slope indicate that samples with small femoral size have higher levels of pelvic dimorphism (negative values father from zero) relative to samples with larger femoral sizes. Although the relationship between femoral size dimorphism and male femoral size is not statistically significant (p ¼ 0.006) at the conservative alpha value (p  0.003), it is at a less conservative alpha of 0.01, and Fig. 3c demonstrates the pattern of larger-bodied samples to show higher femoral size dimorphism than the smallerbodied samples, though with wide scatter. The 95% confidence interval for the slope of this regression line is below 1.0, indicating negative allometry in this relationship.

The patterns of sexual dimorphisms for pelvic and femoral size are similar across the samples in this study in some ways. Based on the indices of sexual dimorphism, males are larger than females (positive indices) for femoral size, and hip bone and ischial length while females are larger than males (negative indices) for dimensions of the planes of the pelvis and pubic bone length; though not all of these differences reach statistical significance in all samples. These results are expected based on previous studies of pelvic dimorphism in humans. Of greater interest are the relationships of pelvic dimorphism in relation to body size (femoral size) and body size dimorphism, or more specifically, the general lack of significant relationships between PSD and femoral size or FSD found in this study. While body proportions vary among the samples, there are moderate but not statistically significant positive correlations between FSD and female and male femoral size (the male femoral size correlation is statistically significant at p  0.01 only). These results do not therefore clearly support previous studies that suggest humans follow the pattern of increasing body size dimorphism with increasing body size (e.g., cf. Wolfe and Gray, 1982; Lindenfors and Tullberg, 1998; Gustafsson and Lindenfors, 2004). The difference in the strength of this relationship when female rather than male femoral size is considered implies that the relationships of PSD on male femoral size may differ somewhat from those presented here for female femoral size. Nevertheless, this study follows the general convention of regressing ISD on female size (e.g., Smith, 1999; Smith and Cheverud, 2002; Lague, 2003). Pelvic dimorphism is not consistent with the expectation of increasing dimorphism with increasing body size; only at a less conservative alpha (p  0.01) do midplane and outlet A-P reach statistical significance. The relationships between PSD and FSD examined in this study provide a means of testing the developmental allometric growth trajectories hypothesis for intraspecific dimorphism. In terms of interspecific patterns of sexual dimorphism, Tague (2005) has shown that for anthropoid primates, species with higher body size dimorphism also have higher pelvic dimorphism, which he suggests results from greater general sensitivity to testosterone in some species relative to others. Extrapolating this model to intraspecific patterns of dimorphism, one might expect that for the samples in the current study, there would be a significant relationship between PSD and FSD, whereby samples with high femoral size dimorphism also have high pelvic dimorphism. The general lack of significant relationships between PSD and FSD found in this study does not match these expectations. In addition, the statistically significant relationship found between inlet M-L dimorphism and FSD illustrates the opposite pattern: samples with high values of PSD have low values of FSD. Only hip bone length dimorphism, which is not considered an obstetrically important dimension, shows the expected pattern of high PSD with high FSD. A possible explanation for low pelvic dimorphism in populations with high body size dimorphism is simply that as males becomes much larger than females (high body size dimorphism), their pelvic size would obviously also increase, and could eventually “catch up” to female pelvic size (low pelvic dimorphism). An alternative explanation for the converse patterns of pelvic and body size dimorphism is that obstetric selection acts to increase the relative size of the female pelvic canal to accommodate birthing a large-brained, broad-shouldered neonate (Tague, 1992; Rosenberg, 1992; Rosenberg and Trevathan, 2002; Kurki, 2005, 2007). Kurki (2007) has shown that in the small-bodied southern African females certain dimensions of the pelvic canal are relatively and absolutely larger for body size than those of larger-bodied Portuguese and EuropeaneAmerican females, which

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Table 5 Regressiona statistics (N ¼ 11) for comparison of indices of sexual dimorphism on female femoral size (ln-transformed). Variable ISD Bi-acetabular Inlet A-P Inlet M-L Inlet posterior Midplane A-P Midplane M-L Midplane posterior Outlet A-P Outlet M-L Outlet posterior Hip bone length Ischial length Pubic length Femoral sizee Femoral size vs. Malef

Pearsonb

p-value

slopec

S.E. slope

95% C.I.

Spearmand

p-value

0.052 0.419 0.435 0.108 0.734 0.172 0.276 0.671 0.092 0.492 0.608 0.316 0.016 0.543 0.762

0.878 0.200 0.182 0.752 0.010 0.612 0.412 0.024 0.787 0.124 0.047 0.343 0.964 0.084 0.006

0.040 0.221 0.282 0.094 0.589 0.169 0.272 0.658 0.111 0.577 0.194 0.127 0.007 0.243 0.262

0.250 0.159 0.195 0.290 0.182 0.323 0.316 0.242 0.399 0.340 0.084 0.127 0.146 0.125 0.074

0.526; 0.606 0.140; 0.581 0.159; 0.723 0.562; 0.751 0.178; 1.000 0.900; 0.561 0.443; 0.987 0.109; 1.206 0.792; 1.014 0.192; 1.346 0.003; 0.385 0.160; 0.414 0.338; 0.324 0.040; 0.526 0.0945; 0.430

0.227 0.400 0.336 0.173 0.763 0.200 0.373 0.736 0.064 0.573 0.718 0.373 0.109 0.473 0.664

0.502 0.223 0.312 0.612 0.006 0.555 0.259 0.010 0.852 0.066 0.013 0.259 0.750 0.142 0.026

a Least squares (model I) regression, pelvic index of sexual dimorphism regressed on female femoral size. Femoral size is the geometric mean of femoral length and head diameter. b None of the Pearson’s correlation coefficients (r) are significant at the conservative alpha (p  0.003). c Slope of the regression line. For regressions with significant correlation coefficients at a less conservative alpha (p  0.01), only femoral dimorphism on male femoral size indicates deviation from isometry (slope ¼ 1.0), as indicated by the 95% confidence intervals. d None of the Spearman’s correlation coefficients are significant at the conservative alpha (p  0.003). e Femoral size dimorphism regressed on female femoral size. f Femoral size dimorphism regressed on male femoral size.

is interpreted as the result of obstetric selection producing a sufficiently large pelvic canal for childbirth. If obstetric selection is acting to protect pelvic canal size in small-bodied populations, one might expect pelvic canal dimorphism to be greater in smallbodied populations. The results of this study do not match this expectation either, again except for midplane and outlet A-P (see above). It may be tempting to interpret the results for midplane and outlet A-P as indicating support for this hypothesis of greater obstetric protection in small-bodied populations influencing pelvic dimorphism, however given the fact that the majority of pelvic canal dimensions in this study do not conform to the expectations under this hypothesis (i.e, there is no relationship between PSD and BSD or body size), this argues strongly that patterns of pelvic dimorphism are not related to body size among human populations. It is interesting then, that Kurki (2007) found that outlet A-P in the small-bodied southern African females is absolutely (and relative to body size) larger compared to the larger-bodied Portuguese and EuropeaneAmerican females. This suggests that while pelvic geometry may vary among human populations of varying body sizes to produce an obstetrically sufficient pelvic canal; these accommodations do not influence pelvic dimorphism. Instead, it may be that male morphology is “pulled along” by selection acting on the female pelvis (e.g., correlated response [Lande, 1980]). In addition, it is important to note that Tague (2005) does not propose that obstetric selection plays no role in the development of pelvic dimorphism in primates; only that selection is not the sole determinant, and the particular dimensions that reflect obstetric adaptations may differ between species. A further consideration is that as these skeletal samples derive from varied geographical regions and time periods, it is likely that any gene flow among the populations would be unequal, which may compromise the independence of each sample. This is a problem for any intraspecific analysis, and indeed many interspecific analyses are affected by phylogenetic relationships among samples. As Gustafsson and Lindenfors (2004, 2009) have shown, applying phylogenetic contrasts to intraspecific human studies of sexual dimorphism in stature results in the disappearance of significant relationships between stature dimorphism and stature. Given that the current study found few significant relationships between PSD and FSD and femoral size, it is unlikely that

phylogenetic contrasts would add significantly to the overall patterns found here. Other factors, particularly locomotor mode, likely play an important role in the development of pelvic size and shape in species. As Schutz et al. (2009b) argue with respect to canid species (and carnivore species in general) locomotive demands for narrow breadths between the hip joints of highly cursorial animals would impinge upon the shape of the pelvic canal. This is also true of primates, who vary extensively in their locomotive modes by species. This may confound interspecific comparisons of pelvic morphology and dimorphism in relation to obstetric selection, particularly given the very divergent pelvic morphology of bipeds in relation to other primate species. Ultimately, the pelvic canal must be large enough for the passage of the neonate, and in every species this demand is met. Non-obstetric factors, such as body size and proportions, locomotive and positional modes, and developmental patterns must certainly contribute to species- and sexspecific pelvic morphology. These findings have implications for the hominin fossil record. Evolutionary changes in body size in fossil hominin species, such as increasing body size in early Homo or the very small-bodied Homo floresiensis, may have impacted dimorphism of the pelvis, particularly in the antero-posterior dimension. Pelvic specimens are relatively rare and often fragmentary in the hominin fossil record. If we cannot estimate the actual levels of dimorphism in the pelvis of extinct species, our ability to reconstruct female pelvic specimens guided by male fossils, and vice versa (Ruff, 1995; Ponce de Leon et al., 2008; Weaver and Hublin, 2009) will be hampered. This may further compromise our understanding of the evolution of hominin childbirth mechanisms. Sexual dimorphism in body size appears to have been high in Australopithecus and Paranthropus, but decreased in Homo erectus and Middle Pleistocene Homo (McHenry, 1994; McHenry and Coffing, 2000; Ruff, 2002, 2010, 2010)). The recently described female pelvis from Gona, identified as a female H. erectus by Simpson et al. (2008) implies that sexual dimorphism may have been much higher in H. erectus than earlier believed, leading Ruff (2010) to question the taxonomic attribution of this specimen. Regardless, there was a significant reduction in body size dimorphism and increase in overall body size in Homo by the Middle Pleistocene, perhaps earlier. The association between FSD

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and inlet M-L dimorphism implies that pelvic dimorphism in Homo may have consequently increased at this time; or given the overall pattern of no association between PSD and FSD, there may have been little impact on pelvic dimorphism as body size dimorphism changed. If this period also coincides with the increase in encephalization and the transition to rotational birth mechanism as proposed by Ruff (1995, 2010), then the patterns of pelvic dimorphism in relation to body size and body size dimorphism in Homo could have changed significantly at this time as well. The effects of thermoregulatory factors on body proportionality and pelvic canal shape in high versus low latitude Middle Pleistocene Homo may also complicate the process of evolutionary change in the human pelvis. Weaver and Hublin (2009) have argued that the broad body of high latitude archaic H. sapiens conserved the wide pelvic canal of earlier Homo, but that low latitude populations, under selection for narrower bodies due to thermoregulatory constraints (Ruff, 1994, 2002), may have undergone reduction in pelvic canal breadth, ultimately leading to the development of the rotational birth mechanism (see also Ruff, 2010). This may also have meant divergent patterns of pelvic dimorphism between high and low latitude populations of Homo. The enigmatic H. floresiensis adds another dimension to the question of the effects of body size change on pelvic morphology of Homo, although this awaits further discovery of pelvic specimens. Finally, the divergent patterns of pelvic and body size dimorphisms found in this study are consistent with other studies that have shown divergent patterns of dimorphisms among craniofacial, pelvic, and body size in inter- and intraspecific studies of mammals (Plavcan, 2003; Cardini and Elton, 2008; Schutz et al., 2009b). The results of these studies imply that the examination of sexual dimorphism in fossil species may be hampered by the choice of skeletal elements for analysis because dimorphism reconstructed from different aspects of the skeleton (e.g., neurocranial vs. facial vs. femoral, etc.) may not be comparable across species. Plavcan (2003) also discusses these issues in relation to the use of different skeletal elements for reconstructing body size in the fossil record. Conclusions

Figure 3. Bivariate graphs of indices of sexual dimorphism [ISD ¼ ln(male/female] on femoral size (ln-transformed), with OLS regression line of best fit with 95% confidence intervals: a) midplane A-P on female femoral size; b) outlet A-P on female femoral size; c) femoral size ISD on male femoral size.

At least two different, yet not mutually exclusive hypotheses have been proposed to explain sexual dimorphism in the size and shape of the pelvis of mammals. The first model argues that selection as a result of obstetric requirements of neonatal cranial size or body mass relative to maternal canal size acts to modify the pelvis of the female (Schultz, 1949; Leutenegger, 1974; Wood and Chamberlain, 1986; Ridley, 1995). The second model posits that differential allometric growth trajectories of males and females, under the influence of growth hormones, lead to intensified pelvic dimorphism as a consequence of high body size dimorphism (Schultz, 1949; Leutenegger, 1974; Tague, 2005). The current study examined the second of these hypotheses in relation to human intraspecific (rather than interspecific) patterns of pelvic dimorphism, based on Tague’s (2005) demonstration that in anthropoid primates, body size dimorphism and pelvic dimorphism are positively related. If this mechanism is working to generate patterns of dimorphism in humans, populations with high body size dimorphism should also display high pelvic dimorphism. However, an overall pattern of no association between pelvic and body size dimorphism was found among human skeletal samples that represent populations of varying body sizes and proportions. These findings are contrary to those expected if pelvic dimorphism in humans is related to overall testosterone sensitivity, as Tague (2005) has suggested for interspecific patterns in anthropoid primates in general.

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With respect to the relationship between pelvic dimorphism and body size in humans, under the obstetric selection hypothesis, one might expect high pelvic dimorphism in smaller-bodied human populations to be generated by stronger obstetric selection, relative to larger-bodied populations. However, only midplane and outlet A-P lengths were found to be associated with femoral size (at p  0.01), indicating that only for these two dimensions do the smaller-bodied samples have higher levels of pelvic dimorphism; one would expect to see more pelvic canal dimensions with higher dimorphism in the smaller-bodied samples. It is important to note that this study did not specifically test the hypothesis that obstetric selection acts to produce patterns of sexual dimorphism across human populations. Finally, an alternative scenario is that as male body size increases, pelvic dimorphism actually decreases as a larger pelvis might scale with larger overall body size. The variability in the relationships of dimorphisms found in this study has additional implications for our understanding of the evolution of body size, sexual dimorphism, and rotational childbirth in Homo. Role of funding source Funding for this project has been provided by the Social Sciences and Humanities Research Council of Canada. SSHRC had no involvement in the planning, carrying out, or decisions on the publication of this research. Acknowledgments I would like to thank the curators who provided access to their collections: Lita Webley and Johan Binneman (Albany Museum,Grahamstown), James Brink (Florisbad Research Station, National Museum, Bloemfontein), Alan Morris (University of Cape Town), Graham Avery (Iziko Museums of Cape Town), Yohannes HaileSelassie and Lyman Jellema (Cleveland Museum of Natural History), Nuno Porto (Museu Antropológico, Coimbra University), Niles Lynnerup (University of Copenhagen), Marta Mirazón Lahr and Mercedes Okurmura (Duckworth Laboratory, University of Cambridge), Marie Besse and Geneviève Perréard (University of Geneva), Patrick Semal (Institut Royal des Sciences Naturelles de Belgique), Monica Zavattaro and Silvia Boccone (Museo di Antropologia e Etnologia, Università degli Studi di Firenze), Giorgio Manzi (Museo di Antropologia, Universita’ di Roma), Philippe Mennecier (Musee de l’Homme), Jerome Cybulski (Canadian Museum of Civilization), Ian Tattersall and Gisselle Garcia (American Museum of Natural History). I would also like to thank Susan Pfeiffer for her helpful editorial suggestions, and S. Leigh and three anonymous reviewers for their excellent and insightful comments. The illustrations for Fig. 1 were produced by Kathryn Killackey Science Illustration and Design. References Abouheif, E., Fairbairn, D.J., 1997. A comparative analysis of allometry for sexual size dimorphism: assessing Rensch’s rule. Am. Nat. 149, 540e562. Arsuaga, J.L., Carretero, J.-M., 1994. Multivariate analysis of sexual dimorphism of the hip bone in a modern human population and in early hominids. Am. J. Phys. Anthropol. 93, 241e257. Badyaev, A., 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol. Evol. 17, 369e378. Berdnikovs, S., Bernstein, M., Metzler, A., German, R., 2007. Pelvic growth: ontogeny of size and shape sexual dimorphism in rat pelves. J. Morphol. 268, 12e22. Berge, C., 1998. Heterochronic processes in human evolution: an ontogenetic analysis of the hominid pelvis. Am. J. Phys. Anthropol. 105, 441e459. Berge, C., Orban-Segebarth, R., Schmid, P., 1984. Obstetrical interpretation of the australopithecine pelvic cavity. J. Hum. Evol. 13, 573e587. Bernstein, P., Crelin, E.S., 1967. Bony sexual dimorphism in the rat. Anat. Rec. 157, 517e526. Bernstein, R.M., Leigh, S., Donovan, S., Monaco, M., 2007. Hormones and body size evolution in papionin primates. Am. J. Phys. Anthropol. 132, 247e260.

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