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Introduction

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

There are several characteristics that set our species apart from other mammals. We are the only living or extant mammal that habitually walks on two legs. For our body size, we have the largest and the most complex brains of all animals. Humans depend on material culture or ‘tools’ for their survival. Humans universally communicate with each other through abstract symbols known as language. Finally, human females routinely seek assistance when they give birth. In fact, many have argued that midwifery or obstetrics, not prostitution, is the ‘oldest profession’. Fossil evidence shows that although two-legged walking, or bipedalism, traces its origin to the very beginning of human ancestry, tools and language appeared much more recently in human evolution. We will argue in this paper that, along with bipedalism, some aspects of the human pattern of birth trace their origin to the very beginning of human evolution.

Based on fossil evidence from Africa, human paleontologists agree that the mammalian family to which humans belong, Hominidae (‘hominids’), originated approximately 5 million years ago1. The crucial hallmarks of our earliest hominid ancestors are skeletal indicators of bipedalism. These markers appear clearly first in Australopithecus anamensis (ca. 4 million years ago)2,3 or possibly earlier4. In spite of a human pattern of locomotion, these early members of the genus Australopithecus had brains that were smaller than modern humans—in proportion to their bodies—very similar to those of modern chimpanzees. Significant brain expansion did not begin until the origin of our genus, Homo, about 2.5 million years ago, when we also have evidence of the first stone tools5. Evidence of language is not directly preserved in the fossil record but several investigators suggest that our ancestors were capable of the complex speech patterns that are part of all spoken languages today by at least 200,000 years ago6. As noted above, we argue that assisted birth may be associated with bipedalism, and may thus be as old as the hominid family itself7. However, assistance at birth is not the only significant birth-related difference between humans and our close relatives in the primate order. The unusual way in which modern humans give birth is the result of a set of constraints imposed by bipedalism, a large brain, and ‘secondary altriciality’, or the delivery of the infant in a relatively helpless state.

Birth in non-human primates

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

Contrary to popular perceptions, humans are not the only animals that have difficulty during childbirth. One important characteristic of primates as a group is a large head and brain relative to body size (i.e. a high encephalisation quotient). For most primates, this means that their neonates at birth have heads that are close to the size of the maternal birth canal through which they must pass. This is especially true of monkeys, lesser apes and humans. The primatologist, Adolph Schultz, depicted this relationship in a classic illustration, redrawn here as Fig. 1, showing the size of the maternal pelvic inlet and the neonatal cranium in spider monkeys (Ateles), proboscis monkeys (Nasalis), macaques (Macaca), lesser apes or gibbons (Hylobates), orangutans (Pongo), gorillas (Gorilla), chimpanzees (Pan) and living humans (Homo)8. The close correspondence between the size of the maternal pelvis and the size of the neonatal cranium is obvious for monkeys, gibbons and humans, whereas orangutans, chimpanzees and gorillas (the great apes and our closest living relatives) appear to have spacious birth canals, probably as a result of their large adult body sizes9 and their relatively small neonates. As one would expect from an examination of these drawings, birth is reported to be difficult for the smaller-bodied primates (monkeys and gibbons) as well as for humans, but somewhat easier for the larger-bodied great apes.

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Figure 1. The relationship between the size of the maternal pelvic inlet and the size of the neonatal head in a range of primate species. Maternal pelvic and neonatal cranial outlines are indicated diagrammatically, but scaled so that the transverse diameters of all maternal pelvic inlets are constant and all other dimensions are scaled as appropriate to the species. For each species, the outlined oval represents the average maternal pelvic inlet, the black oval represents the average neonatal cranium. Note that in the monkeys and the gibbon (Ateles, Nasalis, Macaca and Hylobates) the dimensions of the neonatal cranium are only slightly smaller than the dimensions of the mother's pelvis. In great apes (Pongo, Pan and Gorilla), the pelvic inlet is relatively spacious. In humans, the neonatal cranium is actually longer than the anterior–posterior dimension of the pelvic inlet, requiring the head to enter the inlet facing transversely. Figure is redrawn after Schultz' classic drawing8.

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Although observations of primates giving birth in the wild are rare, we know that neonatal death resulting from cephalopelvic disproportion is not uncommon in the relatively small-bodied species such as marmosets, squirrel monkeys and macaques10. Because the cephalopelvic constraints in monkeys11,12 are greater than those in great apes (i.e. more similar to humans), the comparisons made herein between non-human primates and humans will use monkeys, rather than our closer relatives, the great apes, to represent non-humans.

In all primates, as in humans, the birth canal has three relevant planes, the inlet, the midplane and the outlet. In non-human primates, the three pelvic planes are longer in the sagittal (antero-posterior) dimension than in the transverse dimension. The neonatal cranium is largest in the sagittal dimension in all primate species. Furthermore, the posterior occipital dimension of the neonatal cranium is broad, so that it fits best against the broader posterior portion of the monkey pelvis.

Until recent work by Stoller13, it had been assumed that in monkeys, the sagittal dimension of the neonatal cranium lines up with the sagittal dimension of the pelvis with the neonate facing the ventral side of the mother's body and passing straight through the birth canal without rotating. Thus, it was thought that the monkey neonate is invariably born in an occiput posterior position. Based on observations that included radiographs of laboratory animals during parturition, Stoller has shown that squirrel monkey and baboon neonates may rotate during birth, albeit in a different way than do human neonates. In four baboons (Papio anubis) and seven squirrel monkeys (Saimiri sciureus), Stoller13 found that the neonates entered the birth canal in various positions, but then rotated to exit face first (mentum anterior), facing the maternal pubic bones with their heads in an extended position (Fig. 2).

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Figure 2. Comparison of the entry of the fetal head (in lateral view) into the birth canal in a baboon (left) and a human (right). The figure on the left was drawn from a radiograph taken of Papio anubis (a baboon) by Stoller13. The traditional understanding of monkey birth mechanics was that the neonatal head entered the birth canal with its sagittal axis aligned with the sagittal axis of the mother's body and passed through the birth canal with its occiput against the maternal sacrum, maintaining that orientation through delivery. Stoller13 has shown that in monkeys the neonatal head may enter the pelvic inlet in other positions, such as the one shown here, but that it emerges from the birth canal face first, facing the front of the mother's body. Note that these drawings are not to the same scale. (Figures are drawn from Trevathan10).

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Monkey mothers usually deliver in a squatting position (Fig. 3). As the infant is born, the mother typically reaches down to guide it out of the birth canal and toward her nipples, and may wipe mucus from the baby's mouth and nose to assist its breathing10. Other animals may observe the birth process from a distance, but do not assist the mother or infant. The newborns of most monkey species have sufficiently developed motor skills that an infant can assist in its own delivery once its hands are free.

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Figure 3. A monkey mother assumes various postures during delivery. Three stages in the delivery process are depicted here. Note that the neonate is facing in the same direction as the mother and that the mother is able to reach down and guide the baby easily as it emerges from her birth canal10.

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Monkeys and apes generally give birth wherever and whenever other conspecific group members and predators are least likely to be present10. Labouring mothers typically seek seclusion, often among trees, which provide protection from terrestrial predators. Diurnal species such as monkeys generally give birth at night; nocturnal species such as prosimians tend to give birth during the day14. For non-human primates, birth generally is a solitary event, as it is for most mammals10.

Birth in modern humans

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

As shown in Fig. 1, although the close correspondence between the neonatal cranium and the maternal pelvis in monkeys is also characteristic of humans, the orientation of the pelvic diameters differs. In monkey birth canals, both the inlet and the outlet are greatest in the sagittal dimension, whereas in humans the long axes of the inlet and the outlet lie perpendicular to each other. As noted above, both human and monkey neonate's heads are greatest in the sagittal dimension. The extremely close correspondence between the fetal head and the maternal pelvic dimensions requires that these dimensions line up at all points (inlet, midplane and outlet) during the birth process. In humans, there is an additional challenge to the birth process. In contrast to the narrow shoulders of monkeys, which can pass through the birth canal without rotation, modern humans have broad, rigid shoulders, which generally require the same series of rotations that the head undergoes15. In humans, once the head passes through the outlet, it usually rotates again so that the shoulders can pass through the inlet; further rotation is required so that the shoulders can pass through the outlet.

In addition to the differences in cross sectional shape, human and non-human primate pelvic morphologies differ in another way. The broadest part of the monkey birth canal is posterior, whereas the human birth canal is also spacious anteriorly. As with monkeys, the human neonatal occiput is the largest, most rigid part of its head. Thus, rather than lining up with the back of its head against the maternal sacrum as monkeys do, the human neonate more commonly lies so that its occiput is against the pubic bones, at the front of the pelvis as it exits the birth canal, its convex frontal bone passing along the concave anterior surface of the sacrum16. Additionally, the smallest diameter of the human fetal head is the suboccipitobregmatic diameter. In order to make this minimum cross sectional diameter pass through the plane of maximum diameter of the outlet, the fetal head usually must be flexed as it passes through the outlet and beneath the subpubic arch in an occiput anterior position. This means that the baby generally emerges facing in the opposite direction from the mother (see top drawing in Fig. 3 for the contrasting presentation in monkeys).

This emergence pattern accounts for many unique aspects of human maternal behaviour at birth15. For humans, birth involves other people. Unlike non-human primates, which seek solitude at this time, human mothers actively seek assistance in childbirth. We suggest that this distinction is related to the mechanical differences in the birth process that are the result of the previously discussed anatomic differences. Like non-human primate mothers, human mothers often squat during delivery, although they also assume a wide range of other postures. The most common positions for delivery cited in the anthropological literature are kneeling and sitting. A survey of 159 cultures for which position during delivery was given provides the following data: cultures that prefer sitting, 47; kneeling, 44; squatting, 26; semi-reclining or in a hammock, 17; lying down, 16; standing, 910. Recent studies have demonstrated that, in general, the upright position is optimal for allowing a woman's expulsive efforts to work with gravity in delivering the neonate. The upright position (sitting, squatting or standing) has been shown to result in a shorter second stage of labour, better infant outcomes and fewer negative sequelae for the woman17. When a woman is upright, the presenting part bears most of the force of the neonate's body. The occiput, the most common presenting part, is the most developed of the cranial plates and is best able to withstand this stress. Although the squatting position may be optimal for delivery in that it has been shown to increase intra-abdominal pressure and increase the diameter of the pelvis18,19, very few women, at least in most western societies, have the stamina to remain in this position for the length of time usually required to deliver a child. Squatting during childbirth, however, occurs in cultures in which women spend considerable portions of their time in the squatting position while cooking, visiting, caring for infants and conducting other activities10. Thus, the semi-upright positions of kneeling and sitting represent a balance between the best for expulsion and the most comfortable for the parturient.

Because the human fetus emerges from the birth canal facing in the opposite direction from its mother, it is difficult for the mother, whatever her position, to reach down, as non-human primate mothers often do, to clear a breathing passage for the infant or to remove the umbilical cord from around its neck10. If a human mother tries to assist in delivery by guiding the infant from the birth canal, she risks pulling it against the body's angle of flexion, possibly damaging the infant's spinal cord, brachial nerves and muscles.

The human adaptation to this challenge is to seek assistance during birth10. Today, virtually all women in all societies seek assistance at delivery from relatives, midwives or obstetricians. In a survey of 296 cultural groups in which attendance at childbirth has been described, ethnographers for only 24 such groups noted that delivery may, under certain circumstances, take place unattended. For example, first births may be attended and subsequent ones unattended, or attendance may occur only at births involving complications. Howell20 reported that although giving birth alone is mentioned as a cultural ideal among the !Kung (a hunting–gathering people of southern Africa), most women have their mothers, sisters or other women with them. A woman who gives birth alone arouses interest and concern21. So, while there may be rare exceptions, assisted birth is a phenomenon that comes close to being universal in our species. At some point in the evolutionary past of humans, the advantages of assistance during birth outweighed the disadvantages (e.g. infection or stress resulting from contact with others), so that the species-typical pattern of ‘obligate midwifery’ emerged. Human birth is a social, rather than a solitary event10.

In summary, modern human birth differs from modern non-human primate birth in three fundamental ways: (1) the neonatal head and body generally pass through a series of rotations during birth in response to the close correspondence between neonatal head and shoulder dimensions and maternal pelvic dimensions; (2) the neonate usually exits the birth canal in an occiput anterior position; and (3) human birth occurs in a social context with others in attendance.

When did the human pattern of birth evolve?

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

The series of rotations that the human neonate most commonly undergoes during birth is related to the locomotor pattern of bipedalism as well as to another characteristic aspect of human morphology, a relatively large brain22. These distinctive human features did not appear simultaneously in our evolutionary history, but evolved at different times in response to different sets of selective pressures. The close relationship between the size and shape of the maternal birth canal and the size and shape of the neonatal skull means that in humans and in our immediate ancestors, the mechanism of birth can be inferred from the morphology of the birth canal. Fortunately, some aspects of this morphology are preserved in the fossil record.

The anatomy of bipedalism represents a significant departure from that seen in apes and other non-human primates. Our knowledge of the pelvic anatomy of our earliest bipedal ancestors comes principally from the two best-preserved australopithecine specimens, both sexed as female: Sts 14 from Sterkfontein23, South Africa and A. L. 288-1 (Lucy)24 from Hadar, Ethiopia. These hominids were shorter than modern humans at about 3.5 ft in stature and combined a modern bipedal form of locomotion with a relatively small ape-sized brain. The pelves of both australopithecine specimens are platypelloid (Fig. 4)25,26. Tague and Lovejoy27,28 have shown that, in contrast to the birth canal of modern humans in which the long axes of the inlet and outlet are perpendicular to each other, the long axes of the australopithecine inlet and outlet are parallel to each other. This makes it similar to the straight passageway of the non-human primate birth canal, but with the significant difference in the orientation of its long axis*

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Figure 4. Pelves of a chimpanzee, an australopithecine (the reconstructed pelvis of A. L. 288-1 [‘Lucy’]) and a modern human female. Note the shape of the pelvic inlet. Both hominid inlets are broad transversely, while the chimpanzee is long in the sagittal dimension. The modern human is more spacious in the sagittal plane and therefore more rounded than the early hominid. (Modified from Tague and Lovejoy27).

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Tague and Lovejoy27 suggested that because the australopithecine birth canal had a constant, platypelloid shape throughout its length, there would have been no ‘bony resistance to fetal descent’ and the neonate would have moved through the passageway in a transverse orientation. They argue that rotation of the head within the birth canal would have been unnecessary, given the size of the neonatal head, and impossible, given the platypelloid shape of each pelvic plane.

The mechanism of birth proposed by Tague and Lovejoy is unlike that known for any living animal, and if correct, is an example of the mosaic rather than linear or progressive nature of the evolutionary process. In other words, australopithecines seem to exhibit some aspects of the modern human birth process such as the orientation of the neonatal head in the pelvic inlet, but, according to Tague and Lovejoy, the neonatal head could not rotate as it passed through the birth canal (Fig. 5). This suggests that the characteristically human pattern of neonatal head rotation evolved later in humans as brain size increased, especially in our genus, Homo.

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Figure 5. Comparisons of the mechanism of birth in Pan, A. afarensis and modern Homo. The diagram shows the ‘midwife's or obstetrician's eye’ view of a neonatal head passing through the birth canal. In each drawing, the maternal pelvis and neonatal head are shown in inferior view, with the sacrum at the bottom of the picture and the pubic symphysis at the top. (Modified from Tague and Lovejoy28).

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However, as noted in the description of birth in modern humans, neonatal rotation is not simply a mechanism to accommodate a large cranium. Hominoids (apes, australopithecines and modern humans) have broad, rigid shoulders, which are associated with adaptations of their brachiating or suspensory ancestry. In modern humans, shoulder dystocia is associated with increased mortality for both mothers and infants, especially when the pelvis is platypelloid16. Although this does not present a problem to the large-bodied great apes because of their spacious birth canals, it may have been a source of difficulty that affected the evolution of the birth canal of early hominids. It is possible that after the australopithecine neonatal head passed through the pelvic outlet without rotating within it, the head had to rotate externally so that the wide shoulders could also pass through the pelvic passageway at a 90° angle to the long axis of the head. We suggest that shoulder size may have been an important constraint during hominid birth and, along with increased neonatal cranial size, may have been among the causes of natural selection for the more rounded pelvis of later hominids29. This combination of features resulted from obstetric modifications necessary in a small-brained but broad-shouldered hominid whose pelvic anatomy had been dramatically modified as a result of the shift to terrestrial life and habitual bipedalism.

Birth and encephalisation

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

Because most primates give birth to highly developed (precocial) young, it can be assumed that humans evolved from ancestors who also gave birth to precocial young. Evidence of this can be seen in the fact that humans give birth to single young and the nutritional composition of human milk is like that of other precocial primates30. However, modern human neonates are typically quite altricial (helpless) at birth as compared with infants of other primate species. This observation has led to speculation about the gestation length that would have been characteristic of past hominids. Some authors have suggested that in the past, human gestation was longer, either absolutely or relatively, than it is at present. However, the human 38 weeks of gestation is not very different from the gestation periods of our closest relatives, the great apes—32 weeks for chimpanzees, and 37 weeks for gorillas—and is probably close to the length of the last common ancestor of apes and humans. While undergoing a gestation of nearly the same period as our close relatives, humans are born at a stage of development at which they are more helpless than the neonates of our relatives. Montagu31 referred to the period immediately after the birth of human infants as ‘exterogestation’ suggesting that the human neonate continues for some time to function more as a fetus than an infant. Others have described human babies as being characterised by ‘secondary altriciality’ (that is, they evolved into an altricial pattern from more precocial primate ancestors). Clearly, the extreme helplessness of human newborns has important behavioural implications for such areas as parental behaviour and social relationships.

When did humans begin to give birth to such helpless young? Martin32 proposed that approximately 1.5 million years ago, the size of the pelvis placed a limit on prenatal brain growth, but it was at this time that adult brain size was increasing in our ancestors (e.g. Homo erectus). Two changes could have allowed an increase in adult brain size to occur: human infants could have been born with a smaller percentage of adult brain size (resulting in greater infant helplessness) and/or there could have been an alteration of the shape of the pelvis concomitant with a change in the mechanism of birth. It appears that both of these occurred.

Unfortunately, no complete fossil pelvic remains of known adult female H. erectus individuals have been discovered. However, fossil remains of the pelvis of a young male H. erectus and crania from many other specimens have led scholars to suggest that H. erectus was characterised by a modern human-like pattern of growth in which rapid brain growth continues after birth, rather than an ape-like pattern of growth in which the timing of birth corresponds to a decline in the rate of brain growth33,34. This would mean that, like modern humans, their infants were relatively helpless at birth.

Shoulder dystocia would have necessitated rotation of the head after its passage through the bony birth canal in H. erectus as well as earlier hominids. Hence, these early hominids may have had a rotational form of birth. This rotation may have been different from that in modern humans, however, in that it would have been necessary to accommodate only the broad shoulders and intermediate-sized head of H. erectus rather than both the broad shoulders and large head of the modern human fetus.

By 100,000 years ago our ancestors had evolved essentially modern brain size and pelvic morphology. It can thus be concluded that these archaic humans probably gave birth much as modern humans do35, not only with respect to the mechanism of birth (i.e. rotation of the fetus as it passes through the birth canal and emergence of the neonate from the birth canal in an occiput anterior position), but also in the behaviour associated with birth (i.e. obligate midwifery)10.

A corollary issue that arises from discussion of the evolution of human birth is the question of when the modern human pattern of pelvic sexual dimorphism arose. Modern human sex differences in the pelvis are a reflection of differing balances of the selective constraints on males and females imposed by locomotion and birth. It seems probable that, like the modern pattern of birth, the evolution of pelvic sexual dimorphism took place in a mosaic fashion36.

Birth and human behaviour

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References

One result of the anatomic changes in the pelvis and the associated changes in the ways in which human infants are born is that birth has been transformed from the solitary event that it is for most mammals into a social and cultural event, often marked by culturally specific rules and ritual behaviour. This is, in part, a result of the fact that the human infant emerges from the birth canal facing in the opposite direction from the mother, hindering her ability to assist in its delivery. The presence of another individual who can receive the infant during delivery reduces the risk of mortality for the infant and probably for the mother as well. To put it in evolutionary terms, as bipedalism evolved, natural selection favoured the behaviour of seeking assistance during birth. It is not likely, however, that this was a conscious decision on the part of labouring hominid females. It is more likely that seeking companionship was driven by fear, anxiety, pain or desire to conform to behavioural norms. However, in the long run, seeking another person as an assistant during labour led to reduced mortality, and hence, would have been favoured by natural selection. We argue that the evolutionary process has resulted in heightened emotional needs during labour, which lead women to seek companionship at this time. This suggests that the desire for supportive, familiar people at birth is deeply rooted in human evolutionary history10.

Unfortunately, in many modern hospital deliveries, there is often a mismatch between the evolved needs of women during labour and delivery and the system designed to meet those needs. Too often, women still labour in unfamiliar surroundings with unfamiliar people. Given the depth and long history of the emotions associated with childbirth, it is not surprising that complaints about the modern way of giving birth are common in the United States and other industrialised nations37. The perspective of evolutionary medicine argues that the emotions of childbirth are among the human adaptations to the obstetric complications of bipedalism. Adding to the obstetric team a person whose primary responsibility is to provide social and emotional support to the woman giving birth38 is a reasonable compromise to the mismatch. The roots of this support are as ancient as human lineage itself.

Footnotes
  • *

    The morphologic modifications visible in the fossil postcranial remains and footprints of early hominids occurred because of locomotor rather than obstetric demands. However, these locomotor changes had important consequences with regard to the way that early hominids gave birth.

References

  1. Top of page
  2. Introduction
  3. Birth in non-human primates
  4. Birth in modern humans
  5. When did the human pattern of birth evolve?
  6. Birth and encephalisation
  7. Birth and human behaviour
  8. References
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