Retardation and neotony in human evolution

Dr. D.R.Johnson

Throughout human evolution there has been a tendency to change skull proportions in two ways: first to increase the size of the brain and second to decrease the size of the jaws, jaw muscles and teeth. This has changed the overall shape of the skull: taken together these changes produce a taller skull, with less ridges for muscle attachment and a shorter retrousse face. The position of the foramen magnum has also changed, decreasing the need for powerful neck muscles. These changes produce a striking resemblance between juvenile apes (where many adult characteristics have yet to develop) and man . There is obviously a correlation between increasing brain size and decreasing face size but this is not a simple one since the basic size/shape relationship between ancestral Australopithecines and erectus has broken down in modern man. This resemblance is destroyed during ape development, especially in the male, by strong negative allometry of the brain and strong positive allometry of the jaws . Could man really resemble a juvenile ape, whose allometric growth has been retarded?

This is not a new idea. It was noted in 1836 by Saint-Hilaire a French naturalist who was struck by the behaviour of the first juvenile Orang utan to be shown in Paris Zoo. He retracted an earlier conclusion, based on museum specimens, that young and adult orangs were different genera. The contrast between juvenile and adult skulls were striking - the difference was greater than that between dog and bear.

He attributed these changes to cessation of brain growth, whilst the rest of the skull, i.e. the facial skeleton continued to grow. Behaviour of the young and gentle orang was also like that of man, whilst the adult showed a 'revolting bestiality'. So could the human brain represent an arrest of development?

Politically it was better to think that the Orang had developed too far - i.e. become specialised. The politics were important because we are in an era, the 1830s when recapitulation holds sway and the adult form of each lower creature is supposed to be passed through during the development of man, the pinnacle of creation. The few exceptions to this rule had been noted and discarded as unimportant: but if the development of man disagreed with the theory then it was likely that the theory was at fault. Cope decided that many human features were due to retardation, but quickly added that these were nothing to do with superiority.

In the end it was the theory that had to go, and neotony, the retention of juvenile characteristics became politically correct. Once this was accepted other theories started to appear. Kollmann, inventor of the term 'neotony' paved the way by suggesting that humans evolved from pygmies who had simply retained juvenile features during size increase. The pygmy progenitors probably arose from juvenile apes that had lost the ancestral tendency to regress (as Orangs and Gorillas do).

This was rather odd, but was taken up by Louis Bolk in a long series of papers which argued that man evolved by retaining the juvenile features of his ancestors. Bolk is nowadays unfashionable because his evolutionary views, those of the 1920s are outdated: this is irrelevant. The data will still survive using modern evolutionary theory.

So what did Bolk have on his list of juvenile characters? In his large series of papers is a list

• Flat face
• Lack of body hair
• Loss of pigmentation (Black races are born relatively light: black apes are black at birth)
• Ear form
• Epicanthic eyefold
• Central position of foramen magnum
• High relative brain weight
• Persistence of cranial sutures
• Labia majora
• Structure of hand and foot
• Form of pelvis (not quite sure what he meant here)
• Ventral sexual canal
• Tooth row structure

• Brow ridges
• Cranial crests
• Thin skull bones
• Orbits under cranial cavity
• Brachycephaly
• Small teeth
• Late eruption of teeth
• No rotation of big toe
• Prolonged infantile dependency
• Prolonged growth period
• Long life span
• Large body size (prolongation of fetal growth rate)

But its not a bad theory. In support we can also quote:- 1. the intermediacy of fossil hominids. The structural sequence of A africanus, H erectus, H habilis, H sapiens shows a progressive retention of juvenile forms. 2. the differences in human races. Bolk argued that neoteny had proceeded to different extents in different groups. He had trouble because, as usual, the whites had to come top, and in fact there were strong suggestions in the data that Mongoloids were more neotenous. This led to the unconsciously funny statement
'the white race appears to be the most progressive, as being the most retarded'

So man is a retarded ape.
'man ist einen zur Geschlechtreife gelangten Primatenfetus'
'man is a primate fetus that has become sexually mature'
Bolk 1926.

So what caused this slowing of development which made man's life run like a slow motion film? It must have been an endocrine change . What a come down for man: a sexually mature primate fetus, rendered so by a glandular mutation!

So what is there to dislike in the theory?
Bolk's critics listed
1. the insistence that retardation affects all features to the same extent
2. the placing of the cause as a simple endocrine change
3. the complete absence of any consideration of adaptive significance.

Now most of these arguments depend on Bolk's view of evolution. Along with many others at the time he was not a Darwinian but believed that inner factors controlled evolution, transforming entire organisms along harmonious and definite paths. If evolution were directed by external factors harmony would be impossible because individual characters have different adaptive requirements. Hence Darwinian evolution must be secondary and superficial - mere surface moulding on the underlying internal transformation.

Upright posture, for example might be adaptive, but it arose as a secondary event to fetalisation and retention of the forward position of the foramen magnum.

Because of the flaws in his argument we can reject it: paedomorphosis is not uniform, and not caused by an endocrine event. But when we throw out the bath water of theory we must retain the baby of fact. Bolk was wrong, but his list of retarded features was right. We still have to explain the undoubted neoteny of modern man.

A general temporal retardation of development has clearly characterised human evolution. This has established a matrix in which human evolution must be assessed. The key factor seems to be that retarded development carries with it a set of potential consequences: prolongation of fetal growth rates leading to the retention of juvenile proportions.

So where did this feature arise? Our retardation compared to apes has been accepted, but the general retardation of primates relative to other mammals has been ignored Primates live longer and mature more slowly that other mammals of comparable body size. We reach maturity at 60% of our adult body weight: so do chimps. Most laboratory animals do so at 30%.

The retardation begins early in human development and increases in rate. Otis & Brent compared 147 stage markers in man and mouse: the sequential order of these is essentially the same, but in early embryos are 2-4 times slower in man, later ones 5-15. In physiology the same occurs- in early embryology one mouse day is 4 human days, but later on the ratio is 14 to one as human development slows.

The pattern continues within the primates: apes are larger, slower to mature and live longer than prosimians. Humans go even slower The one important exception to all this is human gestation: this is slightly longer than in apes, but not as much so as we might expect. Are our babies premature?

The general trend in mammalian evolution is from large litters of underdeveloped neonates to small numbers of more developed offspring. Humans are a striking exception: litter size is down, but development is retarded. Relative to the apes our gestation should be around 21 months. A rather startling idea is that this is exactly what does happen: our growth rates are fetal for the first year: we just happen to be extra uterine fetuses. Human growth follows the mammalian norm, but birth happens far earlier than we would expect. Portmann, who suggested this thinks that the reason is that we need to leave the dark unstimulating womb in order to experience sights sounds and smells to help our mental development. He rather dismisses the idea that anything as crude as mechanics might enter into it. But the redesign necessary to allow a woman to give birth to a one year old would be pretty fundamental. As it is humans display the biggest shift from the norm of fetal weight versus maternal weight - it looks small on this slide because of the log scale but the calculated weight is 2200g and the actual 3300g

So we continue to grow at fetal rates, but our development is slowed down: we are big and immature. The skeleton provides a good example of this. Only in man are the epiphyses of long bones and digits cartilaginous at birth: carpel ossification centres are usually lacking in new-borns. In the macaque this state of affairs is present at 18 weeks, and at birth the macaque has the skeletal maturity of a three year old human.

In all other systems too postnatal growth continues past the age of cessation in other primates. The brain grows along the fetal curve: eruption of teeth is delayed maturation is delayed; body growth goes on longer than in any other primate; even senility and death are later. we spend 30% of our life growing.

McKinley has looked at survivorship curves in pre urban man and Australopithecus: they are about the same - so this is not necessarily a new feature.

Perhaps the feature that interests us most is brain growth. In Maccaca the brain is 65% of its adult size at birth, in chimp 40% and in man 23%. Australopithecus is estimated at 25-37%. Chimps and gorillas reach 70% of finical capacity within a year, man takes three. If we plot brain weight against body weight at various ages we find a primate fetal slope of about 1 linked to a postnatal part with a slope of about 0.1 linked by a curved part corresponding to birth. We have this too, but the birth bit is pushed well into postnatal life - about two years. In fact there is just one primate curve, extended in man.

Correlated with the growing brain is a growing skull -or is it that simple? Cranial sutures are certainly delayed in man - the most active period is 25-30 years of age. But circummeatal sutures are still closing in the ninth decade - well after the brain has stopped growing.

So what has been going on? The strong, but hidden assumption in using apes as comparators is that they are appropriate ancestral surrogates. This is almost certainly not so. Many of the features we have 'avoided' by neotony (as compared to the great apes) are in fact specialisations which they have developed. The strong prognathism of the jaw, brow ridges, sagittal crest are all modifications based upon massive dentition. This is as likely to be secondary to a small faced type as our small faced type is to be derived from a simian condition. Quite clearly the trends in development are similar: negative allometry of cranium, positive allometry of jaws, but proceed at different rates. Juvenile forms are, of course, similar. This suggests a way of measuring paedomorphosis: which primate has deviated least from its own juvenile form? We can do this subjectively by taking tracings through skulls .The human skull is larger than the neonate, but the same shape. The orang has grown less, but is a different shape.

A better way is by multivariate analysis. Boyce used 99 skull characters. for male and female and juvenile apes and recent and fossil men. The first principal component split adult apes from adult humans. The second split juveniles from adults. Juvenile apes, humans and Tuang occupy one extreme position, adult apes and Australopithicines the other. Human males and females are close to the juveniles. A cluster analysis places ape juveniles closer to adult man than to their own species.

So what have we learned about man's development? It is retarded. Why? Well, probably it provided a complex of useful features, notably upright posture and large brain. These three developed synergistically . Delayed development has produced a large brain by prolonging fetal growth rates and has supplied a set of cranial proportions suitable for an upright posture. Upright posture freed the hand for tool use and set selection pressures for a larger brain. A larger brain may mean a longer life span. These main elements, as evinced by upright posture and increased brain size have been with us since Australopithecus.

From the child's viewpoint he or she is about as dependent as any in the placental mammals. This dependency is extraordinarily prolonged and the child requires parental care for many years. This has two interlinked consequences: either we can emphasise that it places a premium on learning rather than innate response, or the prolonged childhood provides a better brain with which to learn - really two sides of the same coin. Speech is obviously useful here.

From the parents side there are consequences too. Serial single births with long childhood demand stability and pair bonding. Or perhaps pair bonding is enhanced by a continual stream of dependent children?