Without cesarean delivery, obstructed labor can result in maternal and fetal injuries or even death given a disproportion in size between the fetus and the maternal birth canal. The precise frequency of obstructed labor is difficult to estimate because of the widespread use of cesarean delivery for indications other than proven cephalopelvic disproportion, but it has been estimated that at least 1 million mothers per year are affected by this disorder worldwide. Why is the fit between the fetus and the maternal pelvis so tight? Why did evolution not lead to a greater safety margin, as in other primates? Here we review current research and suggest new hypotheses on the evolution of human childbirth and pelvic morphology. In 1960, Washburn suggested that this obstetrical dilemma arose because the human pelvis is an evolutionary compromise between two functions, bipedal gait and childbirth. However, recent biomechanical and kinematic studies indicate that pelvic width does not considerably affect the efficiency of bipedal gait and thus is unlikely to have constrained the evolution of a wider birth canal. Instead, bipedalism may have primarily constrained the flexibility of the pubic symphysis during pregnancy, which opens much wider in most mammals with large fetuses than in humans. We argue that the birth canal is mainly constrained by the trade-off between 2 pregnancy-related functions: while a narrow pelvis is disadvantageous for childbirth, it offers better support for the weight exerted by the viscera and the large human fetus during the long gestation period. We discuss the implications of this hypothesis for understanding pelvic floor dysfunction. Furthermore, we propose that selection for a narrow pelvis has also acted in males because of the role of pelvic floor musculature in erectile function. Finally, we review the cliff-edge model of obstetric selection to explain why evolution cannot completely eliminate cephalopelvic disproportion. This model also predicts that the regular application of life-saving cesarean delivery has evolutionarily increased rates of cephalopelvic disproportion already. We address how evolutionary models contribute to understanding and decision making in obstetrics and gynecology as well as in devising health care policies.
Cephalopelvic disproportion and obstructed labor
Human childbirth is substantially more difficult than that of most other primate species, owing primarily to the close match between the maternal birth canal and the fetal head ( Figure 1 ). As a consequence of this close fit, even a small variation of maternal and fetal dimensions in human populations leads to a considerable rate of cephalopelvic disproportion (CPD) and obstructed labor.
Where cesarean delivery is not easily available, particularly in developing regions of the Global South (Africa, south Asia, and Latin America), obstructed and prolonged labor are frequent causes of maternal morbidity and mortality. Complications can be short term, such as uterine rupture and chorioamnionitis, or long term, such as fistulas and incontinence. Despite rich epidemiological data on obstructed labor and cesarean delivery, the precise frequency of CPD is difficult to estimate.
Current methods of pelvimetry are unreliable predictors of anatomical disproportion. Apart from an arrest of descent, often a sign of CPD, cesarean deliveries are frequently performed for other indications, e.g., fetal distress, failed induction, arrest of dilatation, repeat cesarean delivery, and maternal request, some manifesting before an arrest because of CPD.
With this complexity in mind, reported CPD rates range from 1% to 8% of childbirths across different geographic regions (World Health Organization, 2003 ). Hence, even the most conservative estimate entails about 40,000 affected births in the United States and about 1.3 million worldwide every year. It is intriguing that childbirth, a process so fundamental to our species’ existence, exhibits such significant complication rates.
Human anatomical traits have been subject to natural selection for millions of years and are therefore often considered to be the best fit available for a given function. Hence, evolutionary anthropologists have long asked the questions: why is the human fetus so tightly matched to the maternal birth canal and thus so prone to birth complications; why is there not a greater safety margin, as in most other primate species ( Figure 1 )?
These long-standing evolutionary puzzles, which are of immediate relevance to obstetrics, gynecology, and public health, have received renewed attention in recent years. Here we review current theoretical and empirical research on the evolution of the human pelvic form and childbirth. Because several recent reviews highlighted the manifold social, cultural, psychological, and legal components underlying obstructed labor and surgical delivery, we focus on the biological aspects and their evolution since the split of the human lineage from the great apes.
The conflicting effects of bipedalism and encephalization on the pelvic architecture
Bipedalism (see Glossary ) evolved in the human lineage 5 million to 7 million years (myr) ago and coincided with a major remodeling of the pelvis. Approximately 2 myr ago it was followed by the massive increase in brain size in the fully bipedal genus Homo , accompanied by an increase in the size of the fetal head.
Studying pelvic evolution throughout time is difficult for several reasons. First, the pelvis is prone to fragmentation and thus poorly represented in the paleontological record. Second, the pelvis is a highly integrated structure, in which selection on any one part results in changes to many others to preserve anatomical and functional integrity. Finally, the human pelvis encountered multiple episodes of different selection pressures, each one leaving traces in the shape of the pelvis that are contingent on previous changes; this challenges the separate reconstruction of these selective forces.
Despite these limitations, there is no doubt that the evolution of bipedalism coincided with major anatomical restructurings of the primate pelvis, as can be seen by comparing pelves of early bipedal hominids, such as australopithecines, to human-like apes ( Figure 2 ). These modifications include the shortening and widening of the illium, the alignment of the sacrum and the pubic symphysis in a dorsoventral plane, the broadening of the sacrum, the development of more prominent ischial spines, and a reduction of the distance between the hip joints and the vertebral column.
Many of these pelvic changes relate to the muscular requirements for efficient upright locomotion and balance of the upright body as well as for support of the viscera. Pelvic changes during the transition to bipedalism also sculpted a very specific birth canal. In australopithecines, the birth canal is mediolaterally broad both at the level of the inlet and at lower levels. Obstetric aspects likely played a minor role in the evolution of the australopithecine pelvis because the skull was relatively small.
Several myr after bipedalism evolved, the pelvis encountered a new evolutionary challenge in the genus Homo : the gradual increase of relative brain size (encephalization, see Glossary ) and, hence, of fetal size. Evolutionary effects of encephalization on the pelvis usually are inferred from comparisons of modern humans to early representatives of the genus Homo , mostly Homo erectus . Even though the cranium of H. erectus is already substantially larger than that of Australopithecus , pelvic differences between australopithecines and H. erectus are likely confounded by co-occurring ecological and behavioral changes that are independent of encephalization, such as changes in body size, ranging behavior, and thermoregulation. It is currently unknown when the increase in brain size started to affect pelvic form, but it is clear that this process continued after the last common ancestor (see Glossary ) with H. erectus .
Relative to modern humans, H. erectus has flaring illiac blades and a mediolaterally broad (platypelloid) birth canal ( Figure 2 ). The prevailing view is that birth-related pelvic changes within the human lineage accounted for the anterio-posterior broadening of the birth canal. Compared with H. erectus , the modern human pelvis is medio-laterally narrower, but this narrowing is relatively recent and appears to have occurred after the adaptation to changed obstetric demands. Finally, modern humans also became taller, which adds another source of strain to the pelvis by increasing the requirements for locomotory musculature and support of the inner organs.
Despite the common evolutionary history and functional demands, pelvic shape varies considerably within and across modern human populations (for the classic types, see Caldwell and Moloy ; Figure 3 ). Studying this variation, along with its functional consequences and complications, can help to determine the manifold roles of the pelvis in locomotion, pelvic floor support, and childbirth, as detailed below.
The concept of an obstetrical dilemma
In 1960, Sherwood L. Washburn introduced the term “obstetrical dilemma” in a review of the effect of tool use on human evolution. Washburn proposed that bipedalism, while freeing hands for tool use, also resulted in the selection for a larger brain given the increasing tool use. Eventually, this led to conflicting selection pressures on the pelvis: concurrent with the evolution of bipedalism, the size of the birth canal had been reduced relative to that of other primates, but the subsequent increase in brain size required a large birth canal.
Such an opposition of selective forces is able to bring net evolutionary change in a trait to a halt, hence the term obstetrical dilemma. Washburn proposed that advantages gained by increased pelvic width are outweighed by biomechanical disadvantages for bipedal gait. For example, individuals with a wide pelvis would have an easier labor and delivery process; however, they would be less successful in gathering food and providing for offspring . Moreover, he reemphasized an idea suggested earlier by Portmann, that the problem of large fetuses was partially ameliorated in human evolution by giving birth at an earlier, more altricial, developmental stage, at which cranial size is smaller.
Whereas primates, in general, are born at an advanced (precocious) developmental stage relative to, for example, mice, this trend is secondarily reversed in the human lineage (secondary altriciality, see Glossary ). Hence, human neonates are more developed than those of truly altricial animals but less developed than those of other primates.
The proposal of Washburn has been highly influential and gained wide acceptance in the anthropological community. The details of this idea, however, have undergone further scrutiny. For simplicity, we will refer to generally wide/broad and narrow pelves in the discussion in the following text, referring to a composite of multiple characteristics, including the width of the birth canal, that make the female pelvis more or less suitable for childbirth (see Figure 4 ). More specific terms will be used when referring to detailed assessments of pelvic shape.
Clearly, a broader birth canal is beneficial for childbirth. This female-specific selection for childbirth is manifested in the strong sexual dimorphism of pelvic anatomy, specifically in the size and shape of the pelvic outlet ( Figure 4 ). In fact, the pelvis is the most dimorphic element of the human skeleton (eg, Fischer and Mitteroecker ).
The source of selection for a narrow pelvis, however, is less clear. Washburn proposed that further widening of the pelvis would impede bipedal gait, but recent biomechanical studies did not support this hypothesis ( Figure 5 ). Warrener and colleagues showed that females and males do not differ in efficiency in either walking or running on a treadmill ( Figure 5 ). The kinematic study of Whitcome et al showed that during walking at higher speed, females translate more of the pelvic rotation into strides than males, which leads to similar efficiency of locomotion despite wider hips. Thus, instead of decreasing efficiency, a wide pelvis contributes to stride length and, particularly in individuals with shorter legs, may even be beneficial for walking.
These findings do not contradict the assumption that human pelvic architecture evolved in response to bipedal gait; they show only that, in modern humans, pelvic width does not considerably affect walking efficiency. This implies that walking efficiency is unlikely to be the cause for the evolutionary retention of our modern narrow pelvis; a broader pelvis, which would clearly ease childbirth, must have other functional disadvantages than only locomotion.
The importance of the pelvic floor
In quadruped mammals and primates, the pelvic floor musculature functions primarily for moving the tail and as sphincter, whereas in upright humans, the muscles and fasciae of the pelvic diaphragm create a horizontal pelvic floor that supports the abdominopelvic organs. It has thus been suggested that maintaining a relatively small pelvic outlet enhances this support function. Anatomical features support this suggestion: the ischial spines, which severely narrow the birth canal in modern humans, serve as attachments of the muscles and fasciae of the pelvic floor ( Figure 6 ). These spines are considerably smaller and located more dorsally in quadrupeds, in which the pelvic floor is a vertical structure, and the weight of the fetus rests predominantly on the backbone. Similarly, the sacral bone protrudes anteriorly into the birth canal in modern humans, whereas it is much shorter and posteriorly oriented in apes.
After the evolution of bipedalism, the importance of pelvic support further intensified with the increase of fetal weight in the genus Homo . Indeed, the ischial spines are less prominent in early hominoids (such as H. erectus , Figure 6 ) than they are in the modern human pelvis, and the modern narrow pelvis likely provides more support for the pelvic floor than the broader archaic one. This evidence suggests that a broad pelvis is more suitable for childbirth but less suitable for carrying the heavy fetus throughout a long pregnancy.
Evolutionarily, this situation intensifies the obstetric dilemma because both carrying and delivering are part of the same process: pregnancy ( Figure 7 ). If gait was the major selective force for a narrow pelvis, walking efficiency might have been compensated for, independently, by changes in leg musculature or behavior. But if pelvic floor support was the crucial driver for a narrow pelvis, such a compensation would not be possible: an evolutionary change that affects one function, either carrying or delivering the fetus, would always affect the other function, too.
Pelvic floor disorders and the obstetrical dilemma
Pelvic floor disorders (PFDs) are common complications associated with pregnancy in general and obstructed labor in particular. The pelvic floor is a complex structure comprised of ligaments, muscles, and fasciae, arranged in several layers. The term pelvic floor disorders refers to a wide range of complications, affecting different parts of pelvic floor architecture and reflecting disruptions of distinct functions.
One group of PFDs arises at birth as a direct consequence of injuries to the muscles of the lower part of the pelvic floor, such as fistulas, uterine rupture, and injury to the sphincter muscles. These injuries are frequent outcomes of prolonged labor as a result of CPD and thus reflect disadvantages of a narrow birth canal, specifically for passing the large fetus during parturition.
According to the pelvic floor hypothesis, another group of disorders is expected to originate from strain to the muscles and connective tissue while carrying the heavy fetus. This strain is more likely to result in complications such as late-onset weakness of ligaments, associated with pelvic floor prolapse and incontinence, as a long-term consequence of multiple pregnancies (although acute injury can also cause these disorders). The strain, a consequence of carrying, is exacerbated when the bony pelvis offers little support and the pelvic floor is weak. Thus, both a wide pelvis during carrying the fetus as well as a narrow pelvis during birthing can result in the same general group of PFDs.
Studies addressing the association between PFD and pelvic anatomy often pool different PFDs to obtain sufficient sample size, but this challenges the detection of associations between specific complications and specific pelvic features. Nonetheless, several studies detected associations of PFD with both a narrow and a wide bony pelvis. For example, in a study of 59 women with PFD and 39 controls, Handa et al found that the transverse diameter of the pelvic inlet is greater in women with pelvic floor disorders than in those without them. Interestingly, they also showed that prolapse is associated with a narrow obstetrical conjugate (the shortest pelvic diameter of the birth canal, see Glossary ), presumably because of a predisposition to injury. Similarly, in a study on 34 patients and 34 controls, Sze et al found that women with vaginal prolapse have a wider transverse diameter of the pelvic inlet than the control group. Two other large studies reported associations of a broad birth canal with urinary incontinence. Stav and coauthors found that women with wide transverse and anterioposterior inlet diameters, as well as with a wider pelvic outlet diameter are more frequently affected by incontinence than women with a narrower inlet. Moreover, Berger et al reported that stress urinary incontinence is associated with a wide subpubic angle and a wide pelvic outlet (large interspinous and intertuberous diameters). Because of the relatively small size of the effect observed, larger samples may be critical given that some of the smaller studies found no differences in bony dimensions. But even weak statistical associations between pelvic shape and pelvic floor function, which may be of limited clinical relevance today, can drive evolution: any consistent association between a morphological trait and survival rate or reproductive success imposes a selective pressure on this trait.
To understand the conflicting selection pressures acting on pregnancy, it will be important for future studies to distinguish between the different disorders and their associations with specific pelvic traits. Such studies may help to predict the risk of certain PFDs based on pelvic anatomy and to develop preventive strategies for women with a wider pelvis, such as strengthening specific aspects of the pelvic floor, introducing external support for carrying, or encouraging behavioral changes that ameliorate unnecessary strain.
The human pubic symphysis is particularly inflexible
Softening and widening of the pubic symphysis as well as relaxation of the sacroiliac joints during pregnancy widens the birth canal and thus ease childbirth; it may appear as a human-specific adaptation to the tight fetopelvic fit.
However, in several other mammals with relatively large neonates, flexibility of the pubic symphysis is much larger than in humans. In guinea pigs, for instance, the mean diameter of the fetal head is 20 mm, whereas the pelvic canal in early pregnancy is just 11 mm wide. To accommodate the fetal head, the pubic bones separate up to 23 mm during late pregnancy in response to estrogen and relaxin, and a ligament appears in the middle of the joint. This flexibility is crucial because calcification of the symphysis, which occurs if the first pregnancy is delayed, frequently leads to CPD in guinea pigs.
The emergence of an interpubic gap, bridged by a flexible ligament, is also a prerequisite for successful delivery in other species, including mice, bats, deer mice, and macaques. In mice, for instance, the gap measures 4–10 mm at delivery, whereas in humans the mean increase of the interpubic gap is only 3 mm. In other mammals, by contrast (eg, in many odd- and even-toed ungulates and in big cats), the pubic symphysis is completely fused by ossification.
Why is the flexibility of the pubic symphysis so variable across mammals, and why is it so inflexible in humans, thus contributive to difficulty in childbirth? A widened pubic symphysis increases the birth canal and thus the vulnerability of the pelvic floor. Most species with a wide pubic gap are either very small and hence experience little pressure on the pelvic floor and engage in postures that reduce force on the pelvis and the pelvic floor (eg, roosting head down in bats), or they reduce the pressure of the viscera and the fetus on the pelvic floor by living in water. An ossified symphysis, by contrast, allows for a higher net force applied by the muscles to the rest of the body and thus may facilitate more energetically efficient locomotion. Apart from many fast-running species, pubic flexibility is also strongly reduced in other large-bodied bipedal species, such as kangaroos.
In humans, a wide symphysis during pregnancy and birth is associated with severe pelvic girdle pain, common among athletes and patients with traumatic pelvic injuries. It is aggravated by weight bearing and associated with difficulty in walking. Evolutionarily, the larger birth canal that would result from increased symphysial flexibility apparently was outweighed by the increased risk of injuries to the pelvis and the pelvic floor. Grunstra et al even hypothesized that bipedal locomotion in humans has not primarily constrained pelvic width, as classically suggested, but the flexibility of the symphysis.
Selection for a narrow pelvis may act via males: a role in erectile function
Both the obstetric demands and the additional strain exerted on the pelvic floor by the heavy fetus are specific to females. The evolutionary trade-off thus differs between the sexes and gave rise to the sexual dimorphism in pelvic morphology and pelvic canal size observable today. Similar dimorphism patterns are also seen in other primate species with a large fetal head relative to the size of the pelvic canal (cephalopelvic index, see Glossary ), such as in lar gibbons, rhesus macaques, and squirrel monkeys, suggesting that pelvic dimorphism is, at least in part, a consequence of fetal size.
It is important to consider the specific conditions required for sexual dimorphism to arise in the evolution of traits that are present in both sexes. Divergent evolution (see Glossary ) of such traits requires opposing selection pressures in the 2 sexes; selection acting in only 1 sex is not sufficient because the developmental genes and processes underlying a trait, in this case the pelvis, are mostly the same whether they find themselves in a male or a female organism (genetic correlation between the sexes, see Glossary ). This means that selection for a broader pelvis in females must have been counteracted by selection for a narrow pelvis in males. If there is no selection in males against the female adaptation, selection in females will also change, at least to a great extent, male shape, and no dimorphism will arise.
The fact that pelvic sexual dimorphism has nevertheless evolved implies that there has been selection opposing the widening of the pelvis in males. Studying the male pelvis may thus provide insights into the advantages of a narrower pelvis independent of disadvantages because of birthing complications. Two relevant selection regimens are plausible: males can either share the same selective pressure for a narrow pelvis with females (as was suggested for gait or for visceral support) but lack the pressure for widening. Alternatively, selection in males may be for a male-specific function, perhaps also indirectly affecting the pelvis in females via a correlated effect.
If pelvic width is associated with pelvic floor strength in males, as is the case in females, male-specific pelvic floor disorders may offer interesting insights. In addition to general effects such as pelvic pain and sphincter dysfunction, one of the disorders associated with a weak pelvic floor in males is erectile dysfunction. The pelvic floor contributes to erectile function by the muscles that form the penile basis, in particular the ischiocavernosus and bulbocavernosus muscles ( Figure 8 ).
