Arch Gynecol Obstet DOI 10.

1007/s00404-011-1918-6

MATERNO-FETAL MEDICINE

The history of vaginal birth

Raphael Camara Medeiros Parente Llian Paglarelli Bergqvist Marina Bento Soares Olimpio Barbosa Moraes Filho

Received: 2 April 2011 / Accepted: 21 April 2011 Springer-Verlag 2011

Abstract Vaginal delivery, as known today, is a still unnished product that originated hundreds of million years ago, much before mammals evolved on land. In this article, we will discuss the way in which our direct ancestors were born over the eons until the present day, focusing on the factors that presented substantial changes in how birth occurred, in relation to our earlier ancestors. The history begins with the rst amniotes around 300 million years ago and ends with the appearance of the rst Homo sapiens around 160,000 years ago. Keywords Mammals Reproduction Placentals Placenta Vaginal delivery

Vaginal delivery, as known today, is a still unnished product that originated hundreds of million years ago, much before mammals evolved on land. In this article, we will discuss the way in which our direct ancestors were
R. C. M. Parente (&) Department of Gynecology, Universidade Federal do Rio Janeiro, 90, CEP: 20.211-340, Rua Moncorvo Filho, Centro, Rio de Janeiro, Brazil e-mail: raphaelcmparente@hotmail.com L. P. Bergqvist Department of Geology, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil M. B. Soares Department of Paleontology and Stratigraphy, Universidade Federal do Rio Grande do Sul, Rio Grande do Sul, Brazil O. B. M. Filho Department of Obstetrics, Universidade Estadual de Pernambuco, Pernambuco, Brazil

born over the eras until the present day, focusing on the factors that presented substantial changes in how birth occurred, in relation to our earlier ancestors. The story begins during the Carboniferous period of the Paleozoic Era. Around 310 million years ago (My), the rst animals with amniotic eggs appeared [1], i.e., the rst to develop embryonic features (e.g., amnion) that continue to be present in human reproduction today. During the Permian period (290248 My), one lineage of amniotes, the synapsids, diversied into several groups (e.g., pelycosaurs, dicynodonts, therocephalians, cynodonts) and, at the end of the Triassic period (215 My), the cynodonts (Fig. 1) developed into our mammal ancestors [2]. Hence, all mammals and the extinct cynodonts form a natural group (bringing together all the descendents from a common ancestor), in the clade Cynodontia [3] (Fig. 2). Several characteristics of the future mammals already existed in cynodonts, such as endothermy, heterodonty (the typical mammalian tooth conguration), possible lactation, greater development of the brain and modications to the cranium, mandible and skeleton that made them increasingly similar to present-day mammals [1]. These changes did not occur all together, but gradually over millions of years. The rst basal mammals (or Mammaliaformes) [4] were extremely small (between 2 and 500 g), insectivores, with nocturnal habits, were endothermic, covered with fur, very agile and had a large brain in relation to the body compared to their antecessors (cynodonts). Morganucodon is taken to be one of the oldest representatives of the mammaliaforms [5] (Fig. 3). The fossils of mammaliaforms do not allow distinguishing whether their reproduction was based solely on eggs, although this was probably the case, given that there are mammals that lay eggs (monotremes) and because of the likelihood that evolution would allow the sequence

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Arch Gynecol Obstet Fig. 1 Skeleton of the Triassic cynodont Thrinaxodon liorhinus. Presacral length is approximately 35 cm (from [1])

Fig. 2 Temporal distribution of cynodonts, mammaliaforms and crown Mammalia. 1 Cynodontia, 2 Mammaliaformes, 3 Mammalia, 4 Australosphenida (including Monotremata), 5 Metatheria, 6 Eutheria (modied from [7])

from oviparity to viviparity, but not the contrary. Therefore, it is very likely that these basal mammals were oviparous [6]. The crown group Mammalia (bringing together all the descendents from the common ancestor of monotremes, marsupials and placentals) was established at the end of the Jurassic period [7] (Fig. 2). The rst divergence occurred

around 166 My ago, when the monotremes followed their own path, as shown by the results of phylogenetic studies based on molecular clocks [8]. The similarities between the mammary glands and secretions of mammals (monotremes, marsupials and placentals) suggest that their common ancestor, probably in the Jurassic period, was able to lactate. The dependence on

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Fig. 3 Mammaliaforms. a Restortation of a primitive mammal based on Morganucodon from Carrol, 1988; b reconstruction of the skeleton of Megazostrodon (from [1]). The animals were 10 cm long to the base of the tail Fig. 4 Eomaia scansoria. a Fur halo preserved around the skeleton; b reconstruction of the skeleton (from [10])

lactation can be inferred from the presence of epipubic bones. These pairs of bones, which articulated with the bones of the pelvis and projected into the abdominal cavity, serve as support for progeny that no longer came out of eggs. They were still present in the advanced cynodonts, in the multituberculate mammals (an extinct group of mammals that lived between 160 and 45 My ago), monotremes and marsupials [9]. These bones no longer exist in presentday placental mammals, but was present in the rst eutherians, such as Eomaia scansoria (Fig. 4), which lived 120 My ago [10]. It is inferred that the rst mammals and multituberculates produced their offspring by means of eggs and/or with a stage in which they went into a pouch,

as in the case of the marsupials [6]. But the use of the epipubic bone as support for progeny that no longer came out of eggs is thought to have been a subsequent development among therians (marsupials and placental mammals). With increasing fetal size among eutherians (placental mammals) consequent to the development of the placenta, this bone became a limitation on fetal size and was lost through evolution [9]. The reproduction of the present-day echidnas and platypuses is based on eggs, but there is an intrauterine period in which endometrial secretions pass through the permeable and elastic shell of their eggs [11]. Monotremes do not have a vagina in the human sense. They use the

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same orice for urinating, defecating and reproducing, which is called the cloaca. Thus, regarding the monotremes, it is still not possible to speak of vaginal delivery. Female monotremes do not have mammary papillae: their milk is secreted by glands located on the abdomen. The marsupials also have a membrane with a shell during the intrauterine period that is supplied by a kind of vitelline placenta [12]. Thus, although marsupials are not called placental mammals, most of them have a kind of choriovitelline placenta formed by the yolk sac. These facts lead to the hypothesis that the placenta came into existence before the divergence between the marsupials and placental mammals (147 My ago) [13]. There are several signs that the placentation of marsupials is highly specialized and cannot be seen as a form that is more primitive to that of eutherians [14]. On the other hand, vitelline placentas may represent an evolutionary event that occurred separately from the predominantly chorioallantoic placentas of eutherians [12]. Marsupials give birth through a vagina, but their progeny are very small and generally less than 5 cm in length [15]. Therefore, there is no difculty whatsoever in delivery and we will not take this type of delivery to be our focus. The placenta is the most diversied organ in the class Mammalia and it contains a wide variety of structures. It is very important to study it to understand how mammalian evolution took place. Since birth after intrauterine development (viviparity) only appeared in therians (marsupials and placental mammals), it is likely that this condition emerged in the last common ancestor among them. On the other hand, as the name indicates, placental mammals have well-developed placentas, which suggests that the common ancestor of eutherians already had a well-developed one [15]. There has been a long discussion aimed at making inferences about what type of placenta this might have been. The most supercial type of placenta is the epithelialchorial type, in which there is no invasion of the uterine wall, but only contact between the chorion and the endometrial epithelium. The epithelial-chorial placenta is seen in animals such as horses and whales, and in some types of primates (e.g., Strepsirrhini or lemurs). A subsequent type with regard to invasion is the endothelialchorial type, in which there is a close relationship between the maternal vessels and the chorion. Finally, in the degree of invasiveness, there is the human placenta, of the hemochorial type, in which there is close contact between the maternal blood and the chorion. This is the most invasive type of placenta [14]. It is also present in other Haplorhini primates, such as tarsiers and the large primates. There are several theories that attempt to identify which placental type was the precursor of the others, and different authors

have advocated each of the types as the ancestral type. The most logical approach would be to think that placentas started with the least invasive nature and progressed to attain the most invasive nature [16]. Nonetheless, placentas may have started with a greater degree of invasiveness and subsequently attained the epithelialchorial type. There are even some authors who have advocated that the endothelialchorial type occurred rst. This discussion has not yet ended. The arguments justifying that the epithelialchorial type came rst are based on the fact that eggs retained in an oviduct would be able to establish supercial contact between the egg and the maternal tissues, thus giving rise to a placental type with low invasiveness [15]. However, since the ancestral divergence between the marsupials and the early placental mammals occurred well before placentas became established in placental mammals, the placenta could have evolved into a more invasive form. Moreover, there are several signs that the placentation of marsupials is highly specialized and cannot be seen as a form that is inferior to that of eutherians [14]. Because of marsupials anatomical differences in relation to placental mammals, such as a lateral vagina and passage of the ureter close to the uterus, in which excessive volume would be an impairment, they had to evolve such that the greater proportion of the development would be based on lactation [17]. Today, although there is still no consensus, it can be said that it is very likely that the ancestral placenta was endothelialchorial or hemochorial, and that the epithelial type derived from one of these. It is universally accepted that the originating ancestors of the placental mammals were very small and produced altricial progeny after a short period of pregnancy. Epithelialchorial placentas are typically found in large animals, with both short and long gestational periods, which make it unlikely that these were the precursors. An intermediate placenta (endothelial chorial) would answer this point. One argument that strengthens this theory is the fact that primates have both extremes of placentation (epithelial and hemochorial). Since these are animals with both long and short gestational periods, it is unlikely that both of these forms of placenta were the primitive form. Therefore, the most accepted theory is that an ancestral endothelialchorial placenta evolved divergently into the two kinds of placentation found in primates, such that the initial placental type among eutherians was endothelialchorial [18]. In fact, as mentioned above, the rst known fossil placental mammal, Eomaia scansoria, was the rst animal about which it is possible to speak of well-established vaginal delivery. Its ilial, ischial and pubic bones were fused; the pelvis was narrow in the sacral joint and vertically deep. The epipubic bone was present, which leads to the belief that the progeny was born in an altricial state

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[10]. These data lead to the belief that the newborns were delivered extremely small and dependent on the mother. Eutherians (placentals) give birth to offspring with a wide variety of altricial development levels or precocial development, although it is believed that the ancestral type was altricial [19, 20] and that precocial birth was derived from this. Among present-day eutherians, an altricial state is found among animals with hemochorial or endothelial chorial placentas, whereas precocial birth occurs among animals with epithelialchorial placentas. The primates (Superorder Euarchontoglires) originated around 90 My ago [8] and are precocial at birth. Human offspring, compared with other primates, are altricial: although their eyes and ears are open at birth, they are extremely dependent on parental care. This may have occurred to support the large human brain, with pregnancy that has to be halted before the end of brain development, such that the neonates have a pattern of brain growth that continues for another year after delivery, For this reason, some authors call human offspring secondarily altricial [21]. The ancestral primates were not large animals, weighing no more than 500 g and having nocturnal and insectivorous habits [22]. Although the oldest fossils date from 55 My ago, biological clock studies have suggested that the rst primates appeared 90 My ago [21]. Primates can be divided into strepsirrhines (lemurs and lorises) and haplorrhines (tarsiers, monkeys, gorillas and humans) or simians (monkeys, gorillas and humans) and prosimians (tarsiers and lemurs), depending on the author [23]. The position of tarsiers is dubious because its primitiveness in various characteristics, such as in the reproductive system, in which they have a bicornuate uterus whereas all simians have a single uterus [24]. Menstruation only occurs in haplorrhines and not in strepsirrhines, probably because the latter do not have invasive placentation [25]. The hypotheses to explain menstruation among primates (among the other mammals, only bats menstruate) include the notions that it serves to expel pathogens carried by spermatozoids or to diminish the metabolic cost of nutrition for an endometrial line constantly prepared for pregnancy, or that it is a side effect from adaptive changes [25]. Copulation at times outside of heat is common among simians, but does not occur among prosimians. At some time between 25 and 40 My [26], the simians split into Catarrhines, including tailless Old World monkeys (great apesgorillas, orangutans and chimpanzees and humans), and Platyrrhines, comprising tailed New World monkeys. At the dawn of Miocene (2316 My ago), the most primitive hominoids, the proconsulids, were a diversied group restricted to the forests of Africa and the Arabian Peninsula. With the aridity established between 17 and

14 My ago, the diversity of the proconsulids diminished and derived hominoids [27] became the dominant taxa. These primates developed new adaptations for feeding and locomotion, but inferences from the fossilized skeletons indicate that they gave birth in a manner similar to the present-day monkeys. Between 13 and 9 My ago, the diversity of hominoids increased with the record of rst hominids. The recovery of few fragmented pelvic bones of Pierolapithecus [28] suggested that the type of delivery of the rst hominids was similar to that of the present-day great apes. The delivery mechanism of humans is very different from that of all other primates. Compared with other catarrhines, humans bear a complex mechanism of fetal rotation inside the pelvic cavity and a fetal passageway inclined forwards, while all other primates have a simple rectilinear mechanism without rotation [29]. Cephalic presentation is the most common orientation, although some smaller-sized species may have facial presentations. Delivery theoretically occurs easily in all large primates (but not in humans) as the birth canal is spacious, probably due to their large body size and relatively small neonates. Some small species may have difculties because of larger fetal size in relation to body size or due to locomotor adaptations [29]. The complex mechanism of human delivery derives from the adaptations to the bipedal posture and great brain size. As an adaptation to large brain size, most of human brain development takes place during the postnatal period, thus differing from other primates. The bipedal posture narrowed the pelvis and shortened the distances between the sacroiliac joints and hip joints. To overcome these problems, the fetal head can ex to diminish the length, with occipital-anterior positioning (in all other primates it is occipital-posterior) and fetal rotation inside the pelvis. After diverging from chimpanzees, the hominins (human lineage) appeared around 7 My ago. It can be supposed from the shape of the femoral head and the position of the foramen magnum (in the posterior region of the cranium) that the primitive hominins were bipedal [30, 31], greatly resembling the australopithecines. This demonstrates that bipedalism is older than had been believed [32], having occurred evolutionally before the process of brain mass development [33]. This has implications for vaginal delivery, even though the volume of the fetal cranium had not yet increased signicantly and was not much bigger than that of a chimpanzee. The rst pelvis for which enough fossil specimens have been found to assure that bipedalism had been adopted is that of Ardipithecus ramidus, which lived 4.4 My ago [34]. In comparison with monkeys and Proconsul, the ilium is expanded mediolaterally and the sacroiliac joint is located more posteriorly. The craniocaudal length of the ilium is

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shorter, and there is a greater lordosis curvature in the lower part of the spine. These changes probably did not bring any changes to the delivery mechanism, because of the small diameter of the fetal cephalic pole. However, narrowing of the pelvis could be observed from the formation of the anteroinferior iliac spine that is absent in chimpanzees. One of the most studied fossils of all times is the 3.2 My old Lucy (Australopithecus afarensis). She was bipedal and had a brain a little bigger than that of a chimpanzee [35]; however, her pelvis was wide compared to other primates and close to the pelvis of Homo sapiens. Her delivery mechanism was rstly described as transverse (without rotation), because there was no bone resistance in the midpelvis [36]. Subsequent studies using new reconstructions of the pelvis demonstrated the current ante-ischial delivery mechanism, including fetal rotation and exion of the cephalic pole, although less accentuated than in the human mechanism and with a less curved fetal passageway [37]. The pelvis of Australopithecus africanus (2.5 My ago) was very similar to the platypelloid of Au. afarensis, although less attened transversally and with an inclined iliac crest [38]. The sacrum was less inclined than that of modern humans [39]. The fetal cranium entered the pelvic inlet obliquely in Au. africanus [39], while it entered transversally [36] or obliquely [39] in Au. afarensis. After exion and rotation, it entered the pelvic outlet sagittally. The australopithecines delivery mechanism anticipates that a small increase in the width at the narrow part would be required for the future cerebral growth of the genus Homo. These could include reducing the biacetabular diameter and increasing the sagittal diameter of the midpelvis and pelvic outlet, given that the present-day basic mechanism with internal and external rotations and exion of the fetal head had already occurred [39]. Australopithecines already had similarities to presentday humans regarding the subpubic angle, small pubic symphysis and mechanics of the resultant forces from the fetal head and pelvic bones. The fetal head, which was not much bigger than that of a chimpanzee, would only be able to come out by means of exion and rotation [39]. The pelvic belt comprises three elements. The two hip bones are joined to the sacrum dorsally (sacroiliac joints) and to each other anteriorly (pubic symphysis), thus forming a ring of bone. All primates have three relevant planes: the pelvic inlet, mid-pelvis and pelvic outlet. In non-human primates, the three planes are greater anteroposteriorly than transversely. In humans, the greater axes in the pelvic inlet and pelvic outlet are perpendicular to each other, given that the pelvic inlet is bigger transversally and the mid-pelvis and pelvic outlet are bigger anteroposteriorly, thus creating the need for rotation movement of the fetal cranium in the birth canal. The human neonatal

cranium is bigger in the sagittal dimension than all other primates. To complicate matters, human shoulders are much broader than in other primates, requiring a further rotation for them to come out. The widest part of the birth canal in monkeys is the posterior part, whereas in humans it is the anterior part. The pelvis of chimpanzees and gorillas is larger than the fetal cranium, thus facilitating passage through the birth canal without the need for rotation and exion. Since the occipital bone is the widest part of the cranium both in monkeys and in humans, delivery generally takes place in an occipital-anterior orientation in humans and an occipital-posterior orientation in monkeys. Small variations regarding the way in which the hip bones are positioned and orientated in relation to the sacrum affect both the format of the pelvic ring (lesser pelvis) and the orientation of the iliac crests (greater pelvis). The human pelvis is much more three-dimensional than is the long attened type of the other primates. The iliac wing is curved forward, thus repositioning the origin of the anterior gluteal muscles and the tensor of the fascia lata, and also altering their extensor function in quadrupeds to hip abductors in bipeds. This is reected in the human femoral head architecture, in which there is less cortical bone in the upper part of the femoral head. This occurs because the anterior gluteal muscles exert compressive stress on this region, thereby impeding tension in this area [33]. Computed tomography scans showed that australopithecines already presented this ossication pattern [33]. It is of fundamental importance to understand the delivery mechanism of humans and other primates to comprehend the profound modications to the pelvis that have taken place over the course of evolution. Two major differences characterize human delivery in relation to that of other primates: fetal rotation and occipital-pubic positioning in most cases. This last detail prevents the mother from helping herself during delivery without the danger of injuring the neonates spinal cord, unlike other primates, which generally give birth alone [40] and in a squatting position. Among non-human primates, the fetus enters the birth canal oriented sagittally, in the same plane as the mothers body, and is delivered in this position, without any rotation, with occipital-sacral positioning in most cases. The pelvic outlet plane in most non-human primates is located behind the ischial tuberosities. In quadrupeds, the sacrum is located above the public symphysis, and thus the fetal head goes beyond the sacrum before entering the pelvic inlet. The fetus goes past the sacrum and the pubis at the same time. The pelvic outlet in non-human great apes is much larger than the fetal head, which means that delivery takes place without difculties. With the evolution of bipedalism, the pelvis was realigned to a greater transverse

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diameter in the pelvic inlet and a greater sagittal diameter in the pelvic outlet. The human fetus typically enters the delivery canal with oblique or transverse positioning, and then rotates by 45 or 135 in order to come out. During delivery, the greatest diameters of fetal presentation (generally cephalic) are adjusted so that they always coincide with the largest maternal diameters [40]. The human delivery mechanism can be summarized as follows: [40] engagement, typically in the oblique or transverse position, as the fetus enters the birth canal; descent, as it passes the pelvic inlet; exion, as the chin is pressed to the chest allowing the smallest cranial dimension to pass rst; internal rotation, so that the head passes through the pelvic outlet in the sagittal dimension and the shoulders enter the inlet in the transverse position; extension, the process by which the head passes under the pubis to emerge in front of the ischial tuberosities; restitution, the process by which the fetal head returns to its original position after having twisted to allow the shoulders to pass through the pelvic inlet in the oblique or transverse position; external rotation, the process by which the head rotates to a transverse position, reecting internal rotation of the shoulders to align in the sagittal dimension of the pelvic outlet; expulsion, which occurs as the anterior shoulder passes under the pubis followed by the posterior shoulder, born by extension over the perineum. This is the usual delivery mechanism in women with a gynecoid pelvis (pelvic inlet broader in transverse dimension). The basic differences in relation to the mechanism in non-human primates are that in the latter, the birth canal is entered sagittally, the sacrum is passed before the pubis, there is no rotation in the pelvic cavity and the fetus comes out in the same orientation as it entered: the fetus emerges behind the ischial tuberosities and does not bend to be born, differing from human fetuses. In humans, the fetus emerges in the front and curves to be born, and birth occurs with occipital-sacral positioning rather than occipital-pubic positioning. Although around 10% of human deliveries occur with occipital-sacral positioning, this is generally in android and anthropoid pelvises, in which the sacroiliac area is broader and better for accommodating the greater dimensions of the fetal occipital bone [40]. The main adaptations of the pelvis of australopithecines were: anterior gluteal muscles became relocated to provide support for the bipedal posture; ilium decreased in anterosuperior length, thus moving the center of mass in front of the hips and knees; retroauricular widening of the ilium made it possible to relocate the gluteus maximus in a position that would allow it to control trunk extension. Other adaptations beyond the pelvis included the position of the foramen magnum more centrally, the increase in the length of the lower limbs in relation to the upper and the improvement of stability of the sole of the foot with loss of

the opposed thumb. These adaptations were fundamental for bipedal locomotion, but did not foreshadow any signicant increase in fetal cranial size. The format of the australopithecines birth canal was platypelloid, i.e., far from the present-day prevalence of the gynecoid form. To allow the passage of larger craniums, the birth canal would have been much wider, more circular and shorter in superoinferior length (to facilitate asynclitism). The changes that led to a larger anteroposterior length also led to a relative reduction in the upper branch of the pubis, which resulted in a more vertical ilium and a smaller femoral head. Several changes led to a larger public inlet and outlet of modern humans: a relative increase in sagittal dimension and an absolute increase in coronal dimension of the pelvis; rotation of the pubis into a higher position and a slight reverse rotation of the ischium. These changes resulted in a greater horizontal axis for the obturator foramen and a smaller inferior deection for the pubis and ischium (which reduced the distance between the ischial tuberosities and the acetabulum), along with creating the obtuse subpubic angle of human females. All of these changes together widened both the mid-pelvis and the pelvic outlet. The ischial spines in monkeys are of insignicant size. However, they became larger in humans and took up a position that made birth difcult: centrally, in the midpelvis. This is the point of greatest constriction during human delivery. This occurred to promote a better attachment point for the ligaments that support the abdominal viscera in the erect position, thereby avoiding prolapses. The pubic symphysis in humans has a unique maturation pattern. Secondary ossication centers do not occur before the end of the third decade of life. This allows the pubic branches to continue to grow even after the remainder of the skeleton has stopped growing and prevents premature fusion of the symphysis before completion of the production of progeny, as could occur in other hominids. These changes are adaptive alterations for delivery that enabled the transition from brains similar to chimpanzees with a volume of around 400 cm [3] to brains of modern humans, with a volume of around 1,400 cm [3]. This largely occurred during the Pleistocene, in the species Homo habilis, H. ergaster and H. erectus [41]. Furthermore, relaxation through hormonal effects on the ligaments occurs during delivery, thereby enabling an increase in the size of the pelvic outlet. This is more pronounced in the anteroposterior dimension than in the transverse dimension. Homo habilis, which lived around 1.9 My ago, had a brain of between 525 and 750 cm [3] (Fig. 5). This was already signicantly bigger than the brain of its australopithecine ancestors, but not yet presenting the very signicant growth that would be seen in H. erectus. The human brain doubled in volume over the period from

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2 million to 700,000 years ago. Body size also increased, but a much greater relative increase occurred over the period from 500,000 to 100,000 years ago, between the last H. erectus and the rst H. sapiens. Delivery of increasingly large brains would be impossible with the old pelvic framework. Thus, evolutionary pressures caused by the increasing brain size forced changes to the pelvic morphology. In addition, other adaptations had to take place, such as neoteny, the delivery at birth of an immature brain with postnatal development. Chimpanzees are born with half of their brain weight, while humans are born with only a quarter of it. The chimpanzees brain stops developing around the age of 4 years, while the human brain only stops developing during adolescence [42]. Another adaptation was the development of great malleability of the skull cap through large fontanelles, a characteristic that is more pronounced in humans than in any other primate. Around 1.5 My ago, with H. erectus, the size of fetal brain started to exert evolutionary pressure for an increase in pelvic size (Fig. 5). At that time, neonates would have started to be born in a more immature state than their ancestors and/or their pelvis will have broadened [43]. Unfortunately, no neonate skull of any ancestral species along the lineage of australopithecines and the rst Homo species are known so far. Consequently, the sizes of the fetal crania of these extinct species have been estimated

based on the relationships between cranial and body size among present-day primates. However, the fossilized pelvis of a young male H. erectus has suggested that this species presented a modern pattern of delivery, with an immature neonate and with an estimated transverse diameter of more than 120 mm for the public inlet in the females of the same species [43]. The transverse narrow pelvis of this species suggests that these were adaptations for better locomotion. An extrapolation to females of the same species suggests that there was no rotation as in humans and it was not possible to deliver fetuses with a large cranium, arguing for a large postnatal cranial development. Recently, a complete female pelvis of H. erectus of 1.4 My to 900,000 years ago was described [44]. Its pelvic inlet was similar to that of modern women, but the mid-pelvis and pelvic outlet were larger. The estimated cerebral volume for its neonates was 315 cm [3]. She still presented several features of australopithecines and may not have had the rotational pattern of modern human delivery, although the pelvis already had adaptations for larger neonatal brains [44]. Another adaptation, but of a social nature, was the establishment of assistance at the time of delivery, not possible for monkeys [44]. With the rotations, the fetus ceased to be born looking at its mother, thereby preventing removal of the umbilical cord or cleaning the airways, and making it impossible for the mother to pull the child out

Fig. 5 Mechanisms of birth in the chimpanzee (left), AL-288-1 (center), and modern human (right). Cephalo-pelvic relationships are shown for the inlet (top), midplane (center), and outlet (bottom). Vault sutures are indicated by dotted lines to show orientation of the fetal cranium. Birth in AL-288-1 was probably simple, in as much as the term fetal cranium was probably of the same approximate size as that of a chimpanzee, and because no reorientation in any of the three stations was required, save for rotation at entrance into the inlet as in humans [41]

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without the danger of hyperextension of the neck with spinal cord damage. Moreover, the neonates of other primates already have enough motor development for them to help in their own births, once their hands are free. In evolutionary terms, at some point of history, assistance at the time of birth became selected as a positive trait, with the positive factors surmounting the negative ones (which may have consisted of infection or anxiety for contact with other people). In this way, delivery ceased to be a solitary event and became a social event [45]. All these changes also gave rise to big differences between male and female pelvises in humans (greater than in other large primates). Men only needed adaptations for bipedalism, whereas women also needed adaptations for childbirth. The subpubic angle in women is greater and the pubic inlet is more oval [46]. These changes were necessary to make possible the passage of larger crania. According to recent estimates [47], the brain volume of Hominidae varied from 400 cm [3] to 1,400 cm [3] (see Fig. 5). The neonatal cerebral volume started with 173 cm [3] in Au. afarensis and reachead around 355 cm [3] in Homo during the Middle Pleistocene [47]. These results demonstrate that the proportion of cerebral growth within the uterus diminished to allow increase in the nal cerebral volume [47]. The Neanderthals, who lived alongside H. sapiens for a long time, may help understand the evolution of human delivery. Although their pelvis and neonatal cranium were similar to those of humans, their delivery mechanism did not include rotation [48]. Considering that they had common ancestors with larger pelvises than in their more remote ancestors, to allow brain development it can be supposed that the decrease in pelvic width in the human lineage (H. sapiens), after the divergence from the Neanderthals, was related to climatic. Neanderthals lived in cold climates while the high temperatures of Africa imposed on H. sapiens a great need for heat loss, which could had been obtained with smaller pelvic dimensions [48]. Fossils of archaic human pelvises consisting of a male specimen found in Spain dating from 600,000 years ago [49] and the largest pre-Holocene human female ever, with an estimated weight of 74 kg, discovered in Jinniushan, China, dating from 260,000 years ago [50], provide evidence for the presence of rotation in the delivery mechanism of these humans. The anatomically modern humans originated in Africa. Fossils from 160,000 years ago, found in Ethiopia, demonstrate intermediate characteristics between archaic and modern H. sapiens [51]. The rst human fossils that are said to be modern date from 93,000 years ago and were found in Israel [52]. The delivery mechanism has not undergone any substantial changes since then, given that the present-day pelvic and cranial volume

measurements differ little from those of the rst modern fossils. Because of the proportions of the maternal pelvis and fetal cranial dimensions, childbirth among modern humans is highly liable to present cephalopelvic disproportion and consequent delayed delivery. Such situations may lead to several complications, such as fetal and neonatal death, maternal death, uterine rupture, vesicovaginal stulas, etc. Millions of years of evolution have not been capable of ending these problems through adaptations to the maternal pelvis and fetal cranium. However, evolution through construction of a more advanced brain in all animals has made it possible for almost all these difculties to be surmounted articially. For the future, this virtually prevents the process of evolution in the form of the maternal pelvis and fetal cranium through the evolutionary pressures that previously existed, given that deaths among women with a pelvis that is less adapted to childbirth hardly ever occurs nowadays, at least in developed countries. We cannot leave evolution in this respect to occur only in poor countries because of a lack of technology for avoiding maternal death due to obstructed delivery. Likewise, we need to do as much as we can to give women the right, with all the necessary care, to give birth to their children in the same way as our ancestors did, if they so wish.
Acknowledgments The authors would like to thank Dr. Kleberson Porpino, from Universidade Estadual do Rio Grande do Norte and Dr. Zhe-Xi Luo from Carnegie Museum of Natural History for protable discussions. Conict of interest We do not have conicts of interests. We have full control of all primary data and we agree to allow the journal to review our data if requested.

Glossary Altricial birth of a fetus before development/ growth has been completed. In neoteny, the physiological (or somatic) development of an animal or organism is slowed or delayed monkeys and apes the most likely ancestors of the genus for Homo of approximately 42.5 mya members of the family Hominidae (or great apes), including the extinct and extant humans, chimpanzees, gorillas and orangutans the great apes such as humans, gorilla, chimpanzee, orangutan and lesser apes (gibbons). Living hominoids are humans, chimpanzee,

Anthropoidea Australopithecines

Hominids

Hominoids (superfamily Hominoidea)

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Hominins Human

K/T boundary

K/T mass extinction event

Old World monkeys

Pelycosaurians

Permian

Precocial

Tetrapods

bonobo, gorilla, orangutan and nine species of gibbon humans and our ancestors, but not other apes Homo sapiens. The word is sometimes also used to refer to any extinct member of the genus Homo (hominins) separation between the age of dinosaurs (Cretaceous 14565 mya) and the age of mammals (Cenozoic). Geologist can nd a worldwide layer of iridium (a rare metal in the earths crust, but common in meteorites) in the geologic strata at 65 mya. K is the traditional geological abbreviation for Cretaceous, the C already being in use for Carboniferous epoch (360300 mya) presumably a large meteorite impact 65 mya near the Yucatan peninsula that caused extinction of all dinosaurs (except birds) and approximately half of all other species a group of primates, from the superfamily Cercopithecoidea. Old World monkeys live in Africa and Asia today, but are also known from the fossil record in Europe. The most familiar species of Old World monkeys are baboons, mandrills and macaques earliest mammal-like reptiles, living in the Carboniferous period. The best known example is the Dimetrodon. Pelycosaurs had a sprawling gait geologic period from 300250 mya that ended, with the most extensive extinction event recorded in paleontology, probably by impact of a comet larger than in the K/T event. In the PermianTriassic event, 9095% of marine species and 70% of all land organisms became extinct refers to species in which the young are relatively mature and mobile from the moment of birth or hatching animals with four limbs, digits, ribs and neck

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