Article (saved from some crap that left from HBF, by Gareth), on neotenism and its biological meaning, written by Ashley Montagu.
lt is the possibility of escaping from the blind alleys of specialization into a new period of plasticity and adaptive radiation which makes the idea of pedomorphosis so attractive in evolutionary theory. Both its possibilities and limitations deserve the most careful exploration.
The unique human trait of always remaining in a state of development is quite certainly a gift that we owe to the neotenous nature of mankind.
In surveying the development of the concept of neoteny it becomes clear that the morphological changes in the varieties of humankind have been brought about mainly by the retention into adult life of traits principally characteristic of the fetus. As Sir Arthur Keith put it, the outstanding structural peculiarities of humankind have been produced during the embryonic and fetal stages of its evolutionary history. It is not so much embryonic as fetal traits, however, that are neotenized both in the evolutionary and individual development of humans. In the evolution of humankind from an anthropoid stock, it is easy to see that gradual change from anthropoid to human could have come about by the retention of the generalized fetal form of the anthropoid into adult stage.
Such retention of anthropoid fetal traits would come about in a mosaic manner, that is to say, not all fetal ancestral traits would be retained in descendant forms but only one or a few at a time. For example, in the australopithecines the front teeth (incisors and canines) underwent reduction, while the teeth at the side and back of the jaws (premolars and molars) retained their large size and only underwent reduction at a later time. The space between the canine (eye-tooth) and the first premolar, the premaxillary diastema, for the reception of the projecting canine of the lower jaw, remained quite wide in the juvenile australopithecine and reduced in later australopithecines. In the pithecanthropines (Homo erectus), a group that may well have originated from australopithecine stock, lhe premaxillary diastema is present in the earliest of the pithecanthropines, Homo erectus robustus, even though it is clear that the canine of the lower jaw had undergone reduction. In short, the space in the upper jaw remained, though it no longer served any useful purpose. Nevertheless, in later pithecanthropines the diastema completely disappeared. Another example of mosaic evolution is that while erect posture was attained by the australopithecines, brain size in the early forms did not appear to change much from that of their anthropoid ancestors. From Homo erectus to Neandertal man, through Solo man of Java, to modern man (Homo sapiens sapiens), we proceed by a steplike process to shed one anthropoid trait after another: the large teeth, projecting jaws, cranial crests, massive eyebrow ridges, and facial structures. Simply by stretching out the fetal stages of development and accelerating the rate of development of the brain, the trend is toward the retention of the structural traits of an ancestral fetus. In Figure 7 in the first column we see the skulls of newborn primates ranging from the rhesus monkey (Macaca mulatta) to a European. We see that all of them closely resemble each other. But reading from the bottom row across from the newbom to the adult male in the last column we can see that in the case of monkey and ape there is a marked change from pedomorphic to gerontomorphic form. Evidence of gerontomorphosis becomes progressively much less marked in the human forms, Neandertal, Australian aborigine, and European. lndeed, in these latter forms, as one progresses from Neandertal to European, the trend is markedly toward pedomorphism, the maintenance of the juvenile form of the skull. This would be even more strikingly evident were it possible to show a series of Chinese skulls ranging from newborn to adult males, for in the adult Chinese skull pedomorphism has proceeded further than in any other people. The Mongoloid skull generally, whether Chinese or Japanese, has been rather more neotenized than the Caucasoid or European: The female skull, it will be noted, is more pedomorphic in all human populations than the male skull; this holds true for many other somatic traits and, I have not the least doubt, for functional and behavioral traits as well. In other words, the female realizes the promise of the species rather more fully than the male.
I have listed some thirty neotenous physical traits in humans; some of these are obviously a reflection of others. For example, the globular form of the skull reflects the great increase in the size of the brain, while flatness of face, small jaws, and small teeth are each closely related to the others. Neotenous functional or physiological traits in humans are many.
THE CRANIAL FLEXURE
In the embryo of all mammals and most vertebrates, Bolk pointed out, the axis of the head forms a right angle with that of the trunk; this is known as the cranial flexure. In all mammals, with the exception of humans, a rotation of the head occurs during the later stages of development so that the head assumes an orientation continuous with the direction of the backbone, as for example in the adult dog. Humans, on the other hand, retain the cranial flexure. The visual axis, the line of sight, of both dog and human is horizontal; however, the dog’s body is also horizontal while that of a human is perpendicular. In the adult great apes, being obliquely quadrupedal, the position of the body is in between, and the axis of the head is also intermediate. The foramen magnum, the aperture at the base of the skull through which the spinal cord passes down into the vertebral canal, is situated rather more posteriorly than it is from the central position it occupies in either fetal ape or human. lt thus transpires that the human erect posture represents the retention in post-natal development of a fetal condition which in other mammals is limited to the period of embryonic or fetal development, that is, a horizontal visual axis and a vertical or perpendicular body. Increase in height and pelvic form are not neotenous, the one being due hypermorphosis, resulting largely from increase in length of the legs, and the other to accommodations to the erect posture.
These are simply statements of fact; they tell us nothing about causation—which is quite another matter, and one upon which we can only speculate. The most probable explanation is that in the evolution of early human the upright posture proved, in the environments in which they found themselves, to be of increasingly great adaptive value. Hence, in such circumstances, changes in the rate of development for the retention of the cranial flexure in relation to the perpendicular body were most likely to be selected.
Against the view that human erect bipedalism has been made possible by the retention of a neotenous fetal relationship between the cranial flexure and body axis is the argument that changes in the pelvic girdle, the lower extremity and foot, and the differences in muscular attachments, especially the gluteus maximus (the large muscles of the buttocks), render it unlikely that neoteny in this connection has any explanatory value whatever. In the first place, it is said, such modifications are never present in the apes, either embryos or fetuses or at any stage of development, and in the second place some of these traits are not even to be found in fetal human. Furthermore, a fundamental feature of the erect bipedal human is the elongated lower extremity, a trait the very opposite of neotenous.
All these criticisms of Bolk’s views are quite sound, but they do not in the least weaken his main argument, for he did not claim that erect bipedalism came into being as a sudden mutation. On the contrary, he appears to have understood that the development of the erect posture was quite gradual. However that may be, the hypothesis of neoteny does not exclude the operation of other factors in the development of the erect bipedal form of locomotion.
When we look at our contemporary primate relatives – the orangutan, the chimpanzee, and the gorilla—and observe the various postures they assume under different conditions, including erect ones, we experience no difficulty in reconstructing the stages through which our ancestors must have progressed to achieve our own erect bipedal posture.
Bolk also drew attention to the fact that the cranial flexure in adult human is paralleled by what de Beer termed the pubic flexure. ln the embryo of mammals the axis of the urogenital structures and rectum is directed downward, but in the adult mammal, with the exception of human, the axis of these structures undergoes rotation so that it comes to lie parallel with the backbone, resulting in a back- ward direction of the vaginal aperture. By contrast, in human the fetal orientation of these structures is retained, so that the vaginal aperture is directed downwards, a principal effect of which is the horizontal face-to-face posture standard in copulation.
THE POSITION OF THE FORAMEN MAGNUM
The central position of the foramen magnum at the base of the skull is another unique human feature among the primates. Interestingly enough, in infant nonhuman primates this foramen is more centrally situated than it is in adults. In these animals, during the growth of the skull, and especially of the jaws and face and the eruption of the teeth, the structure that contributes to the posterior and lateral margins of the foramen, the occipital bone, is pushed, as it were, backwards and upwards, so that the axis of the foramen frequently ends up facing backwards almost in the vertical plane. Fascinatingly enough one of our early progenitors in the line from the pithecanthropines to Neandertal man and so on to ourselves, namely, Soto man from Java, possessed a foramen magnum not quite as centrally situated as in modern humans, the anterior part of which was in the horizontal plane, while the posterior half was almost in the vertical plane. In suckling apes and humans the central portion of the foramen magnum is probably associated with the need for the head to be positioned erectly in nursing at the mother’s breast. Here, too, a flat face is an advantage, owing to the peculiar mechanics of the breast feeding situation. It is for the same reason that the jaws remain undeveloped in all suckling nonhuman primate infants who, like the baboons, will later develop a considerable muzzle. Toward the end of the suckling period in monkeys and apes, when weaning usually commences, the changes in the face and base of the skull lead to the gradual posterior positioning and orientation of the foramen. In humans the fetal position and orientation of the foramen remains unchanged. Hence, the infantile stage of development of these traits, as Keith pointed out, has become permanent in humans. It might be thought, judging from the conditions prevailing in contemporary gatherer-hunter peoples, that the prolonged and intensive breastfeeding enjoyed by children in prehistoric societies, generally lasting some four to seven or more years, had some relation to the development of the erect posture in humans. However, since under natural conditions chimpanzees breastfeed for some five years, the principal factors operative in producing the erect posture have to be looked for elsewhere.
THE FACE AND THE FLEXURE
The bones of the face develop quite independently of those of the rest of the skull. The facial bones are the nasal, maxilla (upper jaw), zygomatic (cheekbones), and mandible (lower jaw). Most of the other large cranial bones contribute to the formation of the brainbox, the sides, back, and base of the skull. The frontal bone also makes its contribution to the face as well as to the sides and base of the skull. The facial bones tend to be vertically inclined in humans, whereas in apes they tend to project in a more obliquely forward direction, largely as a result of the projection of the jaws, a condition called prognathism. In the early fetal development of primates conditions are quite different. In them the cranial flexure is found to be such that the anterior portion of the base of the skull is inclined downward, and the face is similarly inclined beneath the base. In the course of fetal development, however, the flexure straightens out, resulting in the apparent projecting jaws characteristic of all primates with the exception of humans. In humans the fetal flexure is retained, and it is this neotenous condition that accounts for the orthognathy or flat-facedness of humans. These views, using somewhat different terms, were set out by Bolk in a 1923 paper, ‘The Problem of Orthognathism.”
Since orthognathy is confined to the early fetal stages of development in the apes, the neotenous mutations that led to orthognathy must have occurred fairly early in hominid evolution.
These is one feature of the human face which seems rather puzzling. lt is the nose. The human nose is unique among primates, for it juts out like a peninsula left behind by the retreating verticalizing face. In the rush to reduce the prognathic jaw, it would seem, there was a failure to deal with the excess material that remained after the rearrangement of the facial bones. But that is not exactly what happened. Since prognathism makes possible a considerable surface area of vitally necessary mucous membrane within the nasal fossa and its associated structures, reduction of the jaws together with the mucous membranes of the nasal fossa would have constituted a selectively great disadvantage. Hence, the mucous membrane was retained by projecting it outward under cover of that complex organ we call the nose. Whether flat, long, broad, or narrow, whatever its shape, as long as the surface area of the mucous membrane remains adequate for the important functions it is called upon to perform during every moment of the individual’s life, it matters not one bit what the external form of the nose may be.