Sexual dimorphism in the human pelvis: testing a new hypothesis.

Sexual dimorphism in the human pelvis is inferentially related to parturition. Investigators disagree about the identification and obstetric significance of pelvic dimorphism. Benefiting from a large sample of complete skeletons from the Coimbra Identified Skeletal Collection, we show that the dimensions of the true pelvis (birth canal) that are most sexually dimorphic (that is, the dimensions of females are greater than males) are those which are related to biparietal deformation, which often leads to the death of the human neonate. These dimensions are: the anteroposterior diameter of the inlet (index of dimorphism = 108.41), the transverse diameter of the bispinous midplane (index of dimorphism = 117.13) and the transverse diameter of the outlet (index of dimorphism = 112.3). Therefore, sexual dimorphism in the human pelvis is a reflection of differential selection on the two sexes. These results may stimulate further studies with a fresh approach regarding the fossil and comparative evidence for when and how the modern pattern of birth has evolved.     

Kebara 2 Neanderthal pelvis: first look at a complete inlet

The renewed excavations at the Kebara Cave revealed a Neanderthal skeleton dated at about 50-55,000 years B.P. The pelvis of this individual is the most intact Neanderthal pelvis yet discovered, presenting for the first time a complete inlet. Although the superior pubic ramus is extremely long, as typically seen in the Neanderthals, the size of the pelvic inlet is comparable to that of modern Homo sapiens. The length of the superior pubic ramus is found to stem from a more externally rotated innominate bone and not, as generally assumed, from the larger pelvic inlet. It is suggested that the uniqueness of the Neanderthal pelvis may be attributable to locomotion and posture-related biomechanics rather than to obstetric requirements.     

On the differences between two pelvises of Mousterian context from the Qafzeh and Kebara caves, Israel

Two pelvises from a similar archaeological context have been discovered in recent years in two different caves in Israel. The pelvis from the Qafzeh cave (Qafzeh 9) was dated by means of thermoluminescence at approximately 95 kyr BP. All available measurement values, the most significant being those of the diagnostic obturator region, fall within those of the modern range. The other pelvis emanates from the Kebara cave and differs fundamentally from modern pelvises and from the Qafzeh specimen, although the Kebara pelvis is 30,000 years younger than the latter. As in other remains of Neandertal pelvises, the superior pubic ramus of the Kebara hominid is extremely long and slender and exhibits a cross section unlike that of modern humans. The absolute height of the obturator region is very small. It is these measurements and proportions that set the Kebara pelvis apart from both modern pelvises and the specimen from Qafzeh. The morphological differences and the chronological relationship between the two fossil pelvises support the concept of two distinct evolutionary lineages for these hominids.     

Sex differences in the growth of the human bony pelvis

The study of individual patterns of longitudinal growth of the bony pelvic complex reveals the following findings concerning the sex differences in the growth of the bony pelvis. (1) The patterns of growth show the same individual variability and male-female overlap as the adult configuration of pelves. (2) The sex differences in the adult bony pelvis cannot be attributed to the differential response of one bone to sex hormone. (3) Sex differences develop from complicated variations in rates and direction of growth of local areas of the pelvic complex. (4) The superior functional division of the bony pelvis shows only one notable sex difference — the sexual dimorphism of the directional growth of the anterior one-half of the iliac crest. (5) The inferior functional division of the bony pelvis shows numerous local areas of sexually dimorphic growth, but the major sex differences result from the greater lateral migration of the ischia. (6) Of the regions showing definite sexual dimorphism in growth, the pelvic inlet and sciatic notch are the more variable because of their dependency on two separate anatomical systems for their final adult morphological configuration. The subpubic angle and length of the superior pubic ramus are directly associated with only one anatomical system, the enlargement of the pelvic cavity, thus, they show less variability and more definitive sex difference.     

Human hyoid bones from the middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, Spain)

This study describes and compares two hyoid bones from the middle Pleistocene site of the Sima de los Huesos in the Sierra de Atapuerca (Spain). The Atapuerca SH hyoids are humanlike in both their morphology and dimensions, and they clearly differ from the hyoid bones of chimpanzees and Australopithecus afarensis. Their comparison with the Neandertal specimens Kebara 2 and SDR-034 makes it possible to begin to approach the question of temporal variation and sexual dimorphism in this bone in fossil humans. The results presented here show that the degree of metric and anatomical variation in the fossil sample was similar in magnitude and kind to living humans. Modern hyoid morphology was present by at least 530 kya and appears to represent a shared derived feature of the modern human and Neandertal evolutionary lineages inherited from their last common ancestor.     

Adjustment of the fetal head and adult pelvis in modern humans

In nonhuman anthropoids, the anteroposterior (AP) diameters of the fetus are greater than the transverse (TR) diameters and the AP diameters of the pelvic planes are greater than the TR diameters: during labor, therefore, the fetus moves through the birth canal without changing position or orientation. In modern humans, the fetal head at term is encephalized and the fetal chest is flattened. The maternal pelvic inlet is flattened in an AP direction, the sacral promontory and the ischial spines are prominent. As a result, AP<TR at the inlet, but AP>TR at the midpelvis and outlet. In addition, the birth canal presents a marked sacral curvature in the AP direction. The human fetus successfully negotiates the birth canal because the three crucial fetal adaptations: (1) spheroidicity of the presenting part of the fetal head, which allows it to “roll” in the pelvis; (2) mobility of the head and chest in all directions; and (3) a capacity for cranial molding, which adapts fetal head dimensions to pelvic dimensions. The result is that the human fetal head and chest can perform multiple rotational movements in order to always present the greatest fetal diameters to the greatest pelvic diameters. Monkeys show a limited degree of encephalization and suffer from narrow TR pelvic diameters without any possibility of fetal adaptations as shown by humans. Apes also show some encephalization but, because of wider TR diameters in the pelvis, they achieve an easy delivery with no need of fetal adaptations.     

Reconstruction of the STS 14 (Australopithecus africanus) pelvis

The study reports a reconstruction of the sacrum in STS 14 based on extrapolation from the measurements of the first two sacral vertebrae of STS 14 and of the angle formed by the anterior surfaces of their vertebral bodies. Reconstruction is based on comparisons of, and extrapolation from, sacra of Pan troglodytes, Homo sapiens, and Australopithecus afarensis. The reconstructed sacrum has an anterior sacral curvature of 39°. The two ossa coxae were also completed by mirror imaging of one side by the other. With the pelvis completely reconstructed, the pelvic dimensions for the antero-posterior (AP) diameters of the pelvic inlet, midpelvis, and pelvic outlet are 85, 68, and 69 mm and the corresponding transverse (TR) diameters are 109, 88, and 103 mm, respectively. The posterior sagittal diameters in the three pelvic planes are small compared to the anterior sagittal diameters. This analysis indicates that the STS 14 pelvis is platypelloid in the three pelvic planes; i.e., all the AP diameters are smaller than the corresponding TR diameters. This makes the STS 14 pelvis similar to that to Al 288-1, save for a less pronounced degree of platypelloidy at the inlet in the former. © 1995 Wiley-Liss, Inc.     

The postcranial dimensions of the La Chapelle-aux-saints 1 Neandertal

The La Chapelle-aux-Saints 1 Neandertal has figured prominently in considerations of Neandertal body size and proportions. In this context, a reassessment of its major long bones and a reassembly of its principal pelvic elements (sacrum and right ilium) was undertaken. There are secure measurements for its humeral and radial lengths and its femoral head diameter, but the femoral and tibial lengths were almost certainly greater than previous values. The resultant humeral, femoral and tibial lengths are similar to those of other male Neandertals, its femoral head diameter is among the largest known for Middle and Late Pleistocene humans, but its radial length is relatively short. The pelvic assembly provides modest bi-iliac and inlet transverse diameters compared with the few sufficiently complete and undistorted Middle and Late Pleistocene archaic human pelves, but its dimensions are similar to those of large male early modern humans.     

Pubic symphyseal synostosis and sexual dimorphism of the pelvis inPresbytis cristata andPresbytis rubicunda

This study examines the relationship between public symphyseal synostosis and sexual dimorphism of the pelvis in two sympatric species ofPresbytis—P. cristata andP. rubicunda. Whereas no specimen ofP. cristata shows fusion of the interpubic joint, a high percentage of female (43.8%) and male (83.3%)P. rubicunda have a fused public symphysis. As females of both species are similar in body size, they are predicted to give birth to similarly sized newborns. Based on comparison with other anthropoids, the percentage dimorphism in the ischiopubic index inP. cristata andP. rubicuda suggests selection on pelvic capacity in relation to obstetrics. In species characterized by cephalopelvic constriction (i.e., the size of the fetal cranium closely approximates the capacity of the maternal birth canal), successful birth seems possible only by a hormonally induced increase in pelvic joint mobility during delivery. However, fusion of the interpubic joint obviates pelvic joint mobility. Consequently, this study tests the hypothesis thatP. rubicunda shows obstetric adaptations of the pelvis that are not found inP. cristata. The results show that pelvic capacity is larger in females than males in bothP. cristata andP. rubicunda; the sexual difference is most pronounced at the inlet. Moreover, the pattern of pelvic dimorphism is nearly identical between the species. When females of the two species are compared,P. rubicunda evidences a shorter distance between the sacroiliac and hip joints and a wider bituberous diameter. The former is related to interspecific differences in locomotion, and the latter is associated with obstetrics.     

Big-bodied males help us recognize that females have big pelves

Schultz ([1949] Am. J. Phys. Anthropol. 7:401-424) presented a conundrum: among primates, sexual dimorphism of the pelvis is a developmental adjunct to dimorphism in other aspects of the body, albeit in the converse direction. Among species in which males are larger than females in body size, females are larger than males in some pelvic dimensions; species with little sexual dimorphism in nonpelvic size show little pelvic dimorphism. Obstetrical difficulty does not explain this relationship. The present study addresses this issue, evaluating the relationship between pelvic and femoral sexual dimorphism in 12 anthropoid species. The hypothesis is that species in which males are significantly larger than females in femoral size will have a higher incidence, magnitude, and variability of pelvic sexual dimorphism, with females having relatively larger pelves than males, compared with species monomorphic in femoral size. The results are consistent with the hypothesis. The proposed explanation is that the default pelvic anatomy in adulthood is that of the female; testosterone redirects growth from the default type to that of the male by differentially enhancing and repressing growth among the pelvic dimensions. Testosterone also influences sexual dimorphism of the femur. The magnitude of the pelvic response to testosterone is greater in species that are sexually dimorphic in the femur than in those that are monomorphic.     

Variation in pelvic size between males and females

Selection intensity and phenotypic variability are inversely related. It has been hypothesized that, owing to opposing selection pressures on pelvic morphology in females between efficiency in locomotion and obstetric adequacy, female pelvic morphology is less variable than that in males. The hypothesis was supported based on data derived from observational methods of sexing pelves (Meindl et al., 1985). The hypothesis was tested in the present study based on a metrical analysis of the true pelvis. The results show that there are no sexual differences in pelvic variability. Consequently, while males and females are equally variable in the dimensions of the true pelvis, the visual cues that osteologists use to sex pelves are more variable in males.     

Pelvic growth: ontogeny of size and shape sexual dimorphism in rat pelves

The mammalian pelvis is sexually dimorphic with respect to both size and shape. Yet little is known about the differences in postnatal growth and bone remodeling that generate adult sexual dimorphism in pelvic bones. We used Sprague-Dawley laboratory rats (Rattus norvegicus), a species that exhibits gross pelvic size and shape dimorphism, as a model to quantify pelvic morphology throughout ontogeny. We employed landmark-based geometric morphometrics methodology on digitized landmarks from radiographs to test for sexual dimorphism in size and shape, and to examine differences in the rates, magnitudes, and directional patterns of shape change during growth. On the basis of statistical significance testing, the sexes became different with respect to pelvic shape by 36 days of age, earlier than the onset of size dimorphism (45 days), although visible shape differences were observed as early as at 22 days. Males achieved larger pelvic sizes by growing faster throughout ontogeny. However, the rates of shape change in the pelvis were greater in females for nearly all time intervals scrutinized. We found that trajectories of shape change were parallel in the two sexes until age of 45 days, suggesting that both sexes underwent similar bone remodeling until puberty. After 45 days, but before reproductive maturity, shape change trajectories diverged because of specific changes in the female pelvic shape, possibly due to the influence of estrogens. Pattern of male pelvic bone remodeling remained the same throughout ontogeny, suggesting that androgen effects on male pelvic morphology were constant and did not contribute to specific shape changes at puberty. These results could be used to direct additional research on the mechanisms that generate skeletal dimorphisms at different levels of biological organization.     

Sexual dimorphism in the pelvic midplane and its relationship to Neandertal reproductive patterns

The fragmentary nature of the fossil record has limited the analysis of the Neandertal pelvis to the superior pubic ramus and the pelvic inlet. From an obstetric viewpoint, the pelvic midplane or “plane of least dimensions,” defined by the distance between the ischial spines, must be considered in the analysis of hominid reproduction. We examined the relationship between BSD and weight in a mixed sex hospital population undergoing diagnostic computed tomography (CT) scans (41 females and 40 males). Because femoral head diameter squared (FH²) has been used as a proxy for weight in skeletal populations, it was also analyzed with respect to BSD and weight. Bivariate regression analysis of BSD with other body dimensions indicates the presence of significant sex differences. In females, but not in males, weight is a statistically significant predictor of BSD. FH² is an even better predictor of BSD in females while nonsignificant in males. Although weight and FH² are significantly correlated with BSD in females, FH² does not predict weight in females as well as it does in males. The positive correlation between skeletal frame size and BSD in females is indicative of an evolutionary pattern that must take into account the pressures of reproduction. Our results indicate that critical dimensions of the pelvis must increase as the maternal skeleton becomes larger. These results provide a context for the interpretation of the reproductive patterns of a relatively robust hominid population like the Neandertals. © 1996 Wiley-Liss, Inc.     

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

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 small-bodied 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 = 229, female = 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.     

Ontogeny and phylogeny of the pelvis in Gorilla, Pongo, Pan, Australopithecus and Homo

To examine the evolutionary differences between hominoid locomotor systems, a number of observations concerning the growth of the pelvis among the great apes as compared to modern and fossil hominids are reported. We are interested in the size and shape of the coxal bones at different developmental stages across species that may elucidate the relationship between ontogeny and phylogeny (i.e., heterochrony) in the hominoid pelvis. Our hypotheses are: (1) do rates of absolute growth differ?, (2) do rates of relative growth differ?, and (3) does heterochrony explain these differences? Bivariate and multivariate analyses of pelvic dimensions demonstrate both the diversity of species-specific ontogenetic patterns among hominoids, and an unequivocal separation of hominids and the great apes. Heterochrony alone fails to account for the ontogenetic differences between hominids and the great apes. Compared to recent Homo,Australopithecus can be described as 'hyper-human' from the relative size of the ischium, and short but broad ilium. Australopithecus afarensis differs from Australopithecus africanus by its relatively long pubis. In multivariate analyses of ilium shape, the most complete coxal bone attributed to Homo erectus, KNM-ER 3228, falls within the range of juvenile and adult Australopithecus, whereas Broken Hill falls within the range of modern Homo, suggesting that the modern human ilium shape arose rather recently. Among the great apes, patterns of pelvic ontogeny do not exclusively separate the African apes from Pongo.     

Bony pelvic canal size and shape in relation to body proportionality in humans

Obstetric selection acts on the female pelvic canal to accommodate the human neonate and contributes to pelvic sexual dimorphism. There is a complex relationship between selection for obstetric sufficiency and for overall body size in humans. The relationship between selective pressures may differ among populations of different body sizes and proportions, as pelvic canal dimensions vary among populations. Size and shape of the pelvic canal in relation to body size and shape were examined using nine skeletal samples (total female n = 57; male n = 84) from diverse geographical regions. Pelvic, vertebral, and lower limb bone measurements were collected. Principal component analyses demonstrate pelvic canal size and shape differences among the samples. Male multivariate variance in pelvic shape is greater than female variance for North and South Africans. High‐latitude samples have larger and broader bodies, and pelvic canals of larger size and, among females, relatively broader medio‐lateral dimensions relative to low‐latitude samples, which tend to display relatively expanded inlet antero‐posterior (A‐P) and posterior canal dimensions. Differences in canal shape exist among samples that are not associated with latitude or body size, suggesting independence of some canal shape characteristics from body size and shape. The South Africans are distinctive with very narrow bodies and small pelvic inlets relative to an elongated lower canal in A‐P and posterior lengths. Variation in pelvic canal geometry among populations is consistent with a high degree of evolvability in the human pelvis. Am J Phys Anthropol 151:88–101, 2013. © 2013 Wiley Periodicals, Inc.     

Allometric scaling and locomotor function in the primate pelvis

Identification of positional behavior adaptation in the pelvis of primates is complicated by possible confounding effects of body size and phylogeny. Previous work on primate pelvic allometry has focused primarily on sexual dimorphism and its relationship to obstetric constraints in species with large fetal size relative to maternal size. This study investigates patterns of pelvic scaling with a specific aim to understand how pelvic scaling relates to locomotor function. Patterns of scaling of nine pelvic dimensions were examined in a broad comparative sample of 40 species of primates, covering both haplorhines and strepsirrhines, while accounting for phylogenetic nonindependence. Phylogenetic reduced major axis regressions on pelvic scaling patterns suggest that primate-wide patterns are reflected in haplorhine- and strepsirrhine-specific analyses. Many measures scale isometrically with pelvis size, but notably, features of the ilium tend to scale allometrically. As predicted, ilium width and lower ilium cross-sectional area scale with positive allometry, while lower iliac height scales with negative allometry. Further regression analyses by locomotor group suggest that these ilium measures, as well as pubic symphysis and ischium lengths, differ in their scaling patterns according to locomotor mode. These results suggest that scaling differences within primates, when present, are related to functional differences in locomotor behavior and mechanics. This study supports recent work that identifies adaptations to locomotor loading in the ilium and highlights the need for a better understanding of the relationship between pelvic structural mechanics and the mechanical requirements of primate locomotion. Am J Phys Anthropol 156:511–530, 2015. © 2015 Wiley Periodicals, Inc.     

Lower limb entheseal morphology in the Neandertal Krapina population (Croatia, 130,000 BP)

Although the Neandertal locomotor system has been shown to differ from Homo sapiens, characteristics of Neandertal entheses, the skeletal attachments for muscles, tendons, ligaments and joint capsules, have never been specifically investigated. Here, we analyse lower limb entheses of the Krapina Neandertal bones (Croatia, 130,000 BP) with the aim of determining how they compare with modern humans, using a standard developed by our research group for describing modern human entheseal variability. The entheses examined are those of the gluteus maximus, iliopsoas and vastus medialis on the femur, the quadriceps tendon on the patella, and soleus on the tibia. For the entheses showing a different morphological pattern from H. sapiens, we discuss the possibility of recognising genetic versus environmental causes. Our results indicate that only the gluteus maximus enthesis (the gluteal tuberosity), falls out of the modern human range of variation. It displays morphological features that could imply histological differences from modern humans, in particular the presence of fibrocartilage. In both H. sapiens and the Krapina Neandertals, the morphological pattern of this enthesis is the same in adult and immature femurs. These results can be interpreted in light of genetic differences between the two hominins. The possibility of functional adaptations to higher levels of mechanical load during life in the Neandertals seems less likely. The particular morphology and large dimensions of the Krapina enthesis, and perhaps its fibrocartilaginous nature, could have been selected for in association with other pelvic and lower limb characteristics, even if genetic drift cannot be ruled out.     

Morphology and function of the lumbar spine of the Kebara 2 Neandertal

The morphology of the lumbar spine is crucial for upright posture and bipedal walking in hominids. The excellent preservation of the lumbar spine of Kebara 2 provides us a rare opportunity to observe a complete spine and explore its functionally relevant morphology. The lumbar spine of Kebara 2 is analyzed and compared with the lumbar spines of modern humans and late Pleistocene hominids. Although no size differences between the vertebral bodies and pedicles of Kebara 2 and modern humans are found, significant differences in the size and orientation of the transverse processes (L₁‐L₄), and the laminae (L₅, S₁) are demonstrated. The similarity in the size of the vertebral bodies and pedicles of Kebara 2 and modern humans suggests similarity in axial load transmission along the lumbar spine. The laterally projected (L₂‐L₄) and the cranially oriented (L₁, L₃) transverse processes of Kebara 2 show an advantage for lateral flexion of the lumbar spine compared with modern humans. The characteristic morphology of the lumbar spine of Kebara 2 might be related to the wide span of its pelvic bones. Am J Phys Anthropol 142:549–557, 2010. © 2010 Wiley‐Liss, Inc.