REPRODUCTIVE DEVELOPMENT OF THE FEMALE

Ashley Montagu

THE BIOLOGY OF ADOLESCENT STERILITY

The evidence cited in the foregoing pages clearly shows that the immature human female who is less
than 20 years of age conceives much less easily, as a rule, and much less frequently, in general, than the
mature female up to 30 years of age. It is also clear that a high percentage of these younger women are
relatively sterile, and that, in general, prior to the age of 20 ± 2 years the process of childbearing
constitutes a hazard to the life of both mother and child which increases in proportion to the
youthfulness of the mother and decreases to a minimum at maturity.110 All the evidence has pointed
strongly in the same direction, namely, to the conclusion that the adolescent female is biologically
immature, developmentally unprepared, for the processes of reproduction; that when these processes
are early initiated and exercised before maturity is reached the well-being of the mother and of the child
is endangered.

Hal. 161

In young adolescent females there generally exists a colligation of conditions which, in the largest
number of cases, tends to secure such females against undergoing an experience for which biologically
they are inadequately prepared. This is putting the matter somewhat teleologically; it would, perhaps,
be more correct to say that the adolescent organism being itself in process of development is not
generally endowed with the capacity to perform the functions ofreproduction until it has reached a
certain stage of efficient differentiation. This latter stage depends upon the capacity, among other
things, to produce mature ova; and this is a capacity which, as we have seen, there is good reason to
believe is not attained in most mammals until some appreciable time after the appearance of the first
estrus or menarche.

The ontogenetic developmental history of all mammals consists in a process of differentiation in which
organ systems undergo differential development, at rates and in regions that follow one another in a
definite serial pattern, at more or less definite moments of time as determined by the system in which
the developmental process proceeds. The process begins with the fertilization of the ovum and
terminates with the attainment of maturity. In the human female the evidence points to the age of 23 ±
2 years as the age of maturity. The optimal conditions for reproduction prevailing in the organism at that
time, that is, at the age of 23 ± 2 years, are maintained for about five years, at the end of which time,
that is to say between 28 and 30 years of age, the process of involution commences, and at about 45
years of age expresses itself in the menopause. Puberty represents an early transition period in the total
development process, a bridge that leads from childhood to maturity, during which maturation
gradually takes place in certain parts of the reproductive system, and leads to the phase of development
we recognize as maturity, the period when the organism actually becomes capable of efficient
reproduction.

Hal. 162

DEVELOPMENTAL PHYSIOLOGY OF REPRODUCTION

In what immediately follows we shall discuss the develop¬ mental physiology of the primates with
particular reference to the human species insofar as it relates to the functions of reproduction. We must
determine to what extent, if any, the physiological evidence supports the idea of the existence of a
period of adolescent sterility in the primates.

Development consists of growth or increase in size, and differentiation or increase in complexity. At

fertilization the process of development is initiated in the ovum by the spermatozoon; there is
immediate growth and gradual increase in complexity. Throughout the process of development growth
seems to be one step ahead of differentiation. The spermatozoon contributes the determiners of sex in
the form of a specific chromosome-gene structure, which eventually leads to the development of one or
another particular set of sex characters, according as the chromosomal structure is of the male or the
female determining variety. The development of these characters in mammals is brought about by
certain internal secretions, believed to be already present at the so-called “sexually indifferent” stage of
development of the organism: the stage during which the sex of the organism cannot ordinarily be
determined save by reference to its chromosomal pattern.(11) (12)

It appears that from a very early stage in development the general somatic differentiation of the tissues
of the organism proceed together, inseparably. All development, in short, is sexual development, the
distinction between morphologic and sexual development being an arbitrary one. The process of
development consists in the organization of tissues for the fulfillment of certain specific functions:
structures have no other meaning than this, and apart from living the chief function of every organism is
reproduction, and to this end all development would seem to proceed. Tissues and organs undergo
development at rates and in regions that are related to one another in circumscribed serial patterns, so
that one process or event cannot occur without exercising a specific influence upon others within the
system.

Hal. 163

The general pattern of development is such, throughout the animal kingdom, that the functional
qualities of a tissue or an organ are always preceded by growth and increase in complexity in such
tissues and organs. The gradual development of the functions of the somatic system are dependent
upon the rates of growth and differentiation of the tissues comprising it; and in the individual
development of the organism a particular succession of changes must occur before any one of these
functions can be established. So it is with the development of the structures and functions devoted to
the reproductive system. These do not appear in the newborn infant in a state ready for the
performance of the processes of reproduction, but many years must elapse during which the necessary
changes gradually occur that eventually render reproductive activities possible.

The outstanding characteristic of development as a spatio-temporal phenomenon is its gradualness.

At birth the organism is in possession of most of the elements necessary for reproduction. Ova are
present in the ovaries, and the pituitary contains gonadotropic hormones.13 The latter when injected
into older animals are capable of inducing ovulation in them. Anterior pituitary hormones, as a rule, are
incapable of producing ovulation in the newborn animal. As the animal grows, however, ovarian
reactivity to the hormones becomes established, and as sexual maturity is approached the amount of
hormone necessary to produce a given reaction progressively decreases. While the ovary is capable of
reacting to gonadotropic hormones already present in the anterior lobe of the pituitary at a very short
time after birth, under normal physiological conditions it does not do so until long afterwards. It has
been suggested that this is due to the fact that though the pituitary contains gonadotropic hormones at
this early stage, they are not introduced into the blood stream until a later stage of development has
been reached. Since such hormones have been recovered from the urine of two- and three-year-old
children, and from the sera of fetuses,(18) (19) the explanation must obviously be looked for elsewhere.
(14) (24)

Hal. 164

Evidence of a gradually developing sensitivity of the reproductive system to hormonal stimuli is now well
established.(20) (25)

Studies, extended over several years, on basal waking temperature in adolescent girls by Cooperman
from shortly after they had arrived at menarche, indicated that the estrogenic phase of the normal cycle
was associated with low temperature, while the luteal phase was associated with higher temperature.
The rise in temperature occurring in the middle of the average 27 to 31 day cycle coincided with
ovulation. This thermogenic effect is due to the action of progesterone.23 In the female who ovulates a
characteristic biphasic temperature curve is characteristic. When there is no ovulation the temperature
does not rise and the curve is monophasic. Rubenstein found a monophasic temperature curve to be
typical of the menstrual cycles of girls in their early postmenarcheal years.(24)

Doring corroborated these findings in a study of 1,471 menstrual cycles in 303 girls. Basal temperature
studies showed that in the postmenarcheal female the proportion of anovulatory cycles and cycles with
an abnormally short luteal phase is abnormally high. Doring also found that the optimal proportion of
normal cycles was only achieved in the 26 to 30 year age group.(25)

Thus the high proportion of anovulatory cycles in girls before the age of 20 strongly points to the
existence of a normal relative sterility.
Doring’s findings are shown in Table 37. They are based on a total of 3,175 cycles.(26)

In order that a female may conceive and bring the process of pregnancy to a successful termination it is
necessary that her ovaries should be able to produce mature ova capable of being fertilized, then
implanted in the uterus, and there acted upon in such a manner as to cause the fertilized ovum to
undergo development up to the stage when the organism is ready for birth. All these processes require
the presence in the maternal organism of a number of gradually developed conditions. In the absence of
any of these conditions reproduction cannot occur. These conditions come into existence in a regular
order in physiologic and chronologic time, before the establishment of which as a functional complex
the female cannot reproduce. If she is not yet able to ovulate she obviously cannot be impregnated, and
if she is able to ovulate the absence of the luteinizing hormone (LH) or interstitial cell-stimulating
hormone (ICSH) as it is interchangeably known may make it impossible for the fertilized ovum to
become attached to the uterine wall. It is just these two conditions, ovulation and formation of the
corpus luteum, which do not normally be¬ come functionally established until sometime after puberty, if
in the conventional sense we here take puberty to mean the period of the first estrus or first
menstruation.

Van Herwerden, Allen, Hartman, and Corner were the earliest investigators to show that the early
menstruations of the female rhesus monkey are normally unaccompanied by ovulation.(27-31) It is thus
impossible for the early menstrual rhesus female to conceive. There is every reason to believe that the
same conditions hold true for the human female at a similar stage of development.

Hal. 166

It is the hypothalamus that controls the secretions of the pituitary hormones. This control is achieved by
neurosecretions from the area of the median eminence of the hypothalamus to the pituitary. The
hypothalamus is itself subject to the many influences of the higher centers of the brain. (20-21) For each
of the pituitary hormones that acts upon target organs the hypothalamus produces both inhibitory
factors and releasing factors. Specific inhibitory factors pre¬ vent the secretion of significant quantities
of particular pituitary hormones, and specific releasing factors act upon the pituitary to release
individual pituitary hormones. The action of the inhibiting and releasing factors is largely under the
influence of genetic factors in interaction with environ¬ mental conditions such as nutrition, light,
altitude, and socioeconomic factors.

There is a temporal sequence in which the hypothalamic inhibitory and releasing factors, and the
pituitary hormones begin to act in bringing about pubertal, and eventually other, sexual changes. As Dr.
Rose Frisch and colleagues have shown in a series of extended studies, menarche appears to be
signalled by the attainment and maintenance of a critical minimum weight in relation to height (Figures
3 and 4).32-42 In American girls the average weight at menarche is about 47 kg (103 lb) and the average
height is about 158 cm. It seems that it is the relative amount of fat in relation to the lean body mass
that is important; a minimum of about 17 percent fat/body weight being necessary for menarche, and
about 22 percent fat/body weight being essential for the maintenance of regular ovulatory cycles at the
completion of growth at ages 16 to 18 years. Individual girls attain these fat percentages or fat/lean
ratios at varying heights and weights.

Hal. 167

During the adolescent growth spurt, which commences in American girls at about nine and one-half
years at an average weight of about 30 kg (66 lb) estimations show that stored body fat more than
doubles by the time they reach menarche, increasing from growth spurt to menarche by about 120
percent. Body fat at menarche amounts to some 20 to 24 percent of mean body weight. The minimum
level of fatness associated with menarche and its maintenance is about 17 percent of body weight. In
young girls who are recently menarcheal menstrual function ceases when body weight for a particular
height falls below that fatness level. There are, in fact, two minimum weights for a particular height, one
at menarche and one after completion of growth at ages 16 to 18 years. The heavier weight for height is
associated with the maintenance of regular ovulatory cycles at those ages after growth is completed.

Hal. 167 dan 169

For the maintenance of regular menstrual function a heavier minimum weight for height corresponding
to an in¬ creased amount of fat/body weight of about 22 percent of body weight is necessary in girls of
ages 16 and over. Frisch and McArthur, for example, found that the minimum weight for the resumption
and maintenance of regular ovulatory cycles in an 18-year-old girl whose height is 165 cm (55") is 49 kg
(108 lb), whereas the minimum weight for menarche of a girl aged 14 years of the same height is about
43.5 kg (96 lb). The heavier minimum weight for regular ovulatory cycles reflects the increase in fatness
that occurs both in early and late maturing girls from menarche to completion of growth at ages 16 to
18 years. The mean fat gain for both early and late maturers from the beginning of the adolescent spurt
to menarche is about 6.5 kg (14 lb).(43)

As Frisch points out pregnancy has high energy requirements: 50,000 extra calories are needed to
maintain a pregnancy to term, and about 120,000 extra calories are required for lactation over a period
of four months, i.e., at the rate of 1,000 extra calories a day. Hence, the period of adolescent sterility is
one during which the additional fatness level makes for the attainment of stable reproductive ability and
the ability to suckle a child. The level of fatness as represented by body weight of the mother affects the
birth weight of the baby.

Frisch and Revelle have suggested that attainment of body weight in the critical range causes change in
metabolic rate which, in turn, reduces the sensitivity of the hypothalamus to estrogen, and thus alters
the ovarianhypothalamic feedback.

The evidence from both animal and human studies tends to support this explanation of the manner in
which pubertal changes are initiated.(44-63)

What possibly happens at the onset of puberty is this: as the fat level of the body in relation to lean
mass reaches a critical phase it activates what is believed to be a gonadotropin stimulating hormone
which results in the release of the follicle stimulating hormone (FSH) from the pituitary.
Hal. 170

The primary function of the follicle stimulating hormone is to instigate morphological development of
the entire follicle. FSH causes growth of the ovarian follicle and a filling of its central cavity with follicular
fluid containing the hormone estrogen.

When, in experimental animals, the pituitary gland is ablated FSH will not cause the follicles to secrete
estrogen. It is probable that FSH is secreted in both sexes continuously with a minor rise in the female in
the follicular phase, and a sharp increase just before ovulation.

Estrogen is not only responsible for the gradual appearance of the secondary sexual characters but also
for the induction of all those changes in the reproductive tract which result in menstruation. Ovulation,
however, does not and cannot occur as a consequence of the action of estrogen alone. At the onset of
puberty estrogen is alone present in appreciable amount. For ovulation to occur another factor of the
hypothalamus as well as a hormone of the pituitary must come into play: namely, the luteinizing
releasing hormone (LRH) and LH.

One current theory has it that the amygdala of the temporal lobe exerts an inhibiting influence on the
hypothalamic centers which release LRH, and that it is the gradual decline of this inhibitory influence
which is responsible for the onset of puberty. In passing it may be noted that since the amygdala, among
other things, monitors emotional stimuli, it has been suggested that stressful situations may produce
suppression of LRH, so that luteinizing hormone is not re¬ leased, resulting in failure of ovulation and
amenorrhea.

Another explanation is that the rising concentration of a gonadal steroid like estradiol has a positive
feedback on the hypothalamus and causes it to produce LRH. This, in turn, stimulates the pituitary to
release large amounts of leutinizing hormones.

The common belief that menarche constitutes the signal of the girl’s arrival at the ability to reproduce is
in error. Both the development of the secondary sexual characters and the appearance of the first
menstruation are evidences of the action of estrogen upon the tissues of the body particularly involved.

Hal. 171

The girl’s menstrual cycles are anovulatory for a period which on the average lasts about three years.
During this period the female is quite unable to re¬ produce. For reproduction to become possible
further changes in development must occur resulting in the secretion of LH. Only then does it become
possible for ovulation to occur and for a female to conceive.

As we have already seen, this early or primary phase of puberty is of variable duration in any given
population of females, and while it may be related to genetic factors64-65 the expression of these, it is
clear, is subject to modification by environmental factors.

Anatomical proof of the anovulatory character of the first menstrual cycles in the human female has
been given by Laqueur.66-68 He described the case of a girl aged 12 years who died from spontaneous
intracerebral hemorrhage. This girl was in every way perfectly well developed, and was 5 feet 2 inches in
height at death; she had experienced four monthly periods. Examination of the ovaries showed the
presence of only one degenerating corpus luteum, thus indicating that there had been three regularly
recurrent periods from a healthy uterus without ovulation.

Collett and her coworkers have shown that the highest incidence of anovulatory menstrual cycles in
American females occurs during the years from 17 to 19; the length of the cycle is also less constant
during these years than at any other time.69 Again, this evidence indicates that the female in the later
years of adolescence is still in process of development as a reproductive organism. At 17 to 19 years of
age she has still not attained her mature reproductive development. In Table 38 the incidence of
anovulatory cycles in 146 females at various ages is set out.

Ovulation and impregnation become possible only when the second hormone of the pituitary,
luteinizing hormone is poured into the blood stream in sufficient quantity and the ovaries reach the
proper stage of differentiation or sensitivity. This marks the period of nubility, and as more than one
earlier author has pointed out, the period of nubil¬ ity is not to be confused with the earlier period of
puberty.

Hal. 172

We have already seen, in the nonhuman mammals that have been investigated, that nubility generally
follows puberty only after a fairly appreciable amount of time has elapsed. Such evidence as we have for
humans indicates that a similar appreciable interval of time must separate the two events or periods in
the human species.

Evidence of the gradual development of the gonadotropic excretory activities of the anterior pituitary
with the approach to and attainment of adolescence is now available for both sexes. With the
refinement of radioimmunoassays both FSH and LH have been demonstrated in the sera of fetuses,
infants, and children of both sexes. Considerably higher concentrations of FSH occur in the sera of
female than in those of male fetuses. While there is no difference in the concentration of estradiol,
there is a highly significant rise in the concentration of testosterone during the second trimester. The
level of increase is nine times that of the female. Near term there is a decline in circulating
gonadotropins, but this trend is reversed following birth with the rapid decrease in the concentration of
the placentaoriginating human chorionic gonadotropin (hCG) and estrogens in the serum. As Page et al.
suggest, this postnatal surge of gonadotropin in both sexes is probably due to the removal of feedback
inhibition by placental steroids.(11)

Hal. 173

During the first two years the female shows a rhythmic pattern of FSH release, a rhythm which is
repeated in adolescence. Between the ages of three and seven boys and girls continue to excrete a small
but constant quantity of estrogens in the urine. From eight to eleven years of age estrogen excretion by
girls increases, and about one-and-ahalf years before menarche it becomes cyclic, the intensity of the
cycles gradually increasing.14 Such findings indicate that menarche is the culmination of a series of
developing neurohumoral conditions that have been proceeding for some years.

Zuckerman had already summarized and stated these facts in 1936.70 He wrote, “Only the first phase of
the full ovulation cycle is experienced for a long period after the process of reproductive maturation
(puberty) sets in both in man and monkeys. The anterior lobe of the pituitary presumably undergoes
waves of activity during which it elaborates only a follicular-maturation hormone, to cause development
of the ovarian follicles. The hormone produced by the developing follicles causes growth of the uterine
mucosa, and when the wave of pituitary activity comes to an end, the wave of follicular growth it
stimulated also ceases, so that the uterus no longer comes under the influence of the follicular
hormone. As a result, a retrogressive uterine phase sets in and menstruation occurs. The first menstrual
cycles after puberty probably always follow this course, i.e., the first menstrual cycles experienced by
women are usually unaccompanied by ovulation.

“Hence it was that the Trobriand Islanders studied by Malinowski never conceived in their early youth in
spite of unrestricted licence. Hence, too, births rarely occur before the third year of effective marital
relationship in Indian ‘child marriages.’ ”

Hal. 174

Early investigators such as Dorfman, Greulich, and Solomon,(77) Oesting and Webster(78) in
investigations on boys and girls, Catchpole and Greulich79 on girls, and Greulich et al.,80 on boys had all
shown that gonadotropin excretion occurs in small amounts in children three years and over, and that
there is a gradual increase in the amount and frequency of occurrence of such hormones with the
approach of menarche and maturity.15-7173 This has been abundantly confirmed by more recent
investigations.

Incidentally, associated with the increase in the intensity of these cycles of estrogen activity before and
after menarche are certain other physiological changes. Thus Shock81 has shown that with respect to
pulse rate, blood pressure, and basal metabolism menarche produces no sudden alteration that is
reflected in these conditions, but that the rate of change, generally a decrease in rate, occurs in many
girls six to 12 months before menarche.(74) “The changes,” writes Shock, “in all the physiological
functions measured are in the direction of adult values and take place at a more rapid rate after
menarche than before.” As shown in Shock’s curves (Fig. 5), three marked changes are associated with
the beginning of menstruation: (1), a leveling off of a premenarcheal rise in systolic blood pressure, (2), a
decrease in pulse rate, and (3), a precipitous fall in basal heat production per unit of surface area. Such
changes, as Shock suggests, are to be regarded as but another aspect of the process of maturity rather
than the result of endocrine changes associated with menstruation.

Puberty, it cannot be too often repeated, is not marked by the first menstruation in the female, nor is it
represented by a single characteristic phenotypic change. Puberty is, in fact, a long drawn-out process
which begins some two years before the first menstruation, externally announced by the growth of
pubic hair and breast development. In the male testis growth and pubic hair appear before the onset of
the pubertal spurt in height.(75)
Hal. 175

An operationally useful definition of puberty is that offered by Donovan and Van der Werff ten Bosch, as
“the phase of bodily development during which the gonads secrete hormones in amounts sufficient to
cause accelerated growth of the genital organs and the appearance of secondary sexual characters.”20
To which I would add, “and the appearance of cyclic bleeding in the female.”

As we have seen, much more is involved in the causation of pubertal changes than gonadal secretions,
as Van der Werff ten Bosch make abundantly clear. Those changes are, in fact, the effects of the
combined operation of genetic, hypothalamic, endocrine, and growth factors.

Hal. 176

It is not our task to consider those factors in any further detail here; they must however be borne in
mind as fundamentally significant in the development of the complex process that puberty represents.
The traditional conception of puberty as marked by the first menstruation must be abandoned, for
puberty is a complex phase of developmental change which lasts some five or more years.

That an appreciable period of time separates the ability to procreate from the appearance of the first
menstruation had already been clearly recognized by Aristotle 2,300 years ago and a century ago by
such physicians as Waddy, Joulin, Matthews Duncan, and others, but the scientific world was quite
uninterested in the matter. The problem has become of more general scientific interest only in recent
years, and it has remained for modern experimental re¬ search in the physiology of sexual development
and reproduction of other mammals and in humans to rediscover and provide the scientific
demonstration of the truths first stated by earlier investigators. In the present chapter an attempt has
been made to provide something of the nature of that scientific demonstration.

Hal. 177

THE PSYCHOLOGICAL AND PHYSIOLOGICAL IMMATURITY OF THE YOUNG MOTHER

In the preceding pages of this book we have seen that the evidence indicates that the adolescent female
is biologically insufficiently developed to carry on the various functions of reproduction in a viably
efficient manner. Prenatal accidents of various sorts and maternal and infant mortality rates are
disproportionately high. Not only is the adolescent female physiologically unprepared, but in most cases
she is behaviorally unready for the task of maternity. Adolescent female mice tend to kill or devour their
newborn offspring more frequently than do mature female mice,* while adolescent chimpanzee
mothers are generally quite incompetent to handle their newborn.(1-3)

Hal. 191

It would seem that behavioral maturation is quite as dependent upon physiological factors as is purely
reproductive maturation. Here, too, there is evidence of some variation. Some very young mothers
appear to handle their young well enough, but there can be little doubt that in general younger mothers
fail to do so. Among human beings the example and instruction of older, more experienced females
plays an important role in assisting the younger mothers to care properly for their children, but even so
very young mothers are notoriously indifferent as compared with more mature mothers.

Evidence of the unreadiness of the adolescent to act as a responsible parent, is the finding of Dorothy
Nortman that childhood mortality at ages one to four is 41 percent above average among children born
to adolescent mothers.(4)

Mental development often appears to be seriously compromised in the children of adolescents. A

Canadian study cited by Nortman found an increased prevalence of handicapped children of adolescent
mothers, and a study of mental defectives found them over-represented among mothers under the age
of 20 and over the age of 35. The J-shaped curve of risk stands out in high relief for young mothers,
being lowest for women in their twenties, and higher for older mothers.

In the immature gravida iron stores, total skeletal stores, trace minerals, and vitamin A are substantially
lower than in the adult female. From animal studies we know that inadequate vitamin A leads to
increased teratogenesis. Giroud considers pregnancy in adolescence a contributing factor in the
production of developmental defects of nutritional origin.5-6

A study, reported by Dr. Janet Hardy from the Johns Hopkins Child Development Study, on the
development of 525 children born to girls who were 16 years or under at the time of delivery, found
that at age four 11 percent of the children scored 70 or below on IQ tests compared with only 2.6
percent of the general population of four-year-olds. While in the general population approximately a
quarter of four-year-olds will test out at 110 and above, only 5 percent of the children born of very
young mothers tested that high.

Hal. 192

School failure and behavior problems were also more pre¬ valent in the study population. Dr. Hardy
goes on to say, “Other serious problems such as child abuse, delinquent behavior and early pregnancies
among the children them¬ selves have been encountered. Yet some of the young mothers and their
children have been successful. These mothers have completed their schooling, hold good jobs, have
established satisfactory family life and their children are doing well and should be successful also.’’7

In short, as Dr. W. H. Baldwin says in her excellent survey of the subject, “To say that there are greater
risks for children born to adolescent mothers does not mean, of course, that all such births will lead to
problems any more than to say that delaying a birth until the twenties will guarantee that child a
splendid life. We can say that the risk of negative outcomes for the pregnancy, the birth, or for the
child's development are higher the younger the mother. Postponing a birth until a woman is in her
twenties offers noticeably decreased risks in all respects.”

In nonhuman mammals it has been shown that prolactin plays a highly important role in producing
maternal behavior in such animals, whether they have themselves recently given birth to young or not.9
It is quite probable that the maternal inadequacies of the immature female are due at least in part to
insufficient concentration of prolactin in her blood stream. This explanation would accord very well with
all that we know concerning the physiological mechanism of adolescent sterility. However this may be,
one of the best indications of the unpreparedness of the adolescent female organism for reproduction
would appear to lie in the high mortality rate of infants born to young mothers, and also in the high
maternal death rate of young mothers.1

But this is only a partial explanation, for there is good evidence that in all mammals maternal behavior is
the result not exclusively of biochemical factors but of the reciprocal interaction between biochemical
and social processes occurring within the mother.12,13 As Brody put it, maternal behavior in animals
“appears to involve physiological responses to instinctual organic needs—for nourishment, warmth,
equilibrium, memory, and learning. And it appears to become explicable without reference to inborn
adaptive mechanisms or to teleological purposes.

Hal, 193

It is highly probable that physiological sexual maturation is correlated with emotional maturity and
awareness of interpersonal relations, for these traits together with intellectual and emotional
functioning have been found to be more highly developed in post- than in premenarcheal females.15

The secular trend toward earlier menarche (which appears to have ceased since the fourth decade of
this century) doubtless contributes to the development of emotional, sexual, and heterosexual interests
at an earlier age than was the case in previous generations. This is a possibility which has not yet
received the attention it deserves.(16)(18)

The relation between age at menarche and personality has been investigated by Shipman in 82 white
American females with a mean age of 39 years. He found that the girls who reached menarche at 10 and
11 years, tended as adults to be more conservative and uncritical in their thinking, more lax and inexact,
more trusting of others, and more group dependent. The middle menarche group, who attained
menarche at age 12 and 13, tended to be more feminine, and to have a higher average number of
children. The late menarche group, who attained menarche at 14 and older, were more dominant and
aggressive, more given to critical thinking and ready to experiment, they were also more suspecting and
self-controlled.(19)

The suggestion here is not that there is a genetic correlation between age at menarche and personality,
but that social conditionings in the form of different responses, choices, and commitments during
adolescence in relation to early or late menarche, may play a significant role in influencing personality
development.

Buck and Stavraky found a positive and significant relationship between age at menarche and age at
marriage for women in maternal age groups 25 to 19 and 30 to 34, but no such relationship in age group
35 to 39. The observations, made on 42,298 women, showed that there was a marked correlation
between early menarche and early age at mar¬ riage.20
Hal. 194

In addition, further evidence of the physiological un¬ readiness of the young mother for childbirth is the
high frequency of toxemias and eclampsia. Marchetti and Menaker, in 634 young mothers ranging in age
from 12 to 16 years inclusive (all blacks with the exception of seven whites) at the Gallinger Municipal
Hospital of Washington, D.C., found the following frequency of toxemias in relation to age (Table 39). Of
these females 93.7 percent were primagravidas.

From Table 39 it will be seen that the frequency of toxemia increases with the youthfulness of the
mother. Comparing these frequencies with the incidence of toxemias in older mothers at the clinic, a
great disparity is observed in favor the clinic group as compared with the young mothers (Table 40).

Hal. 195

SUMMARY AND CONCLUSIONS

The evidence presented in the preceding chapters strongly supports the view that in the females of the
mammals thus far investigated, mouse, rat, hamster, sheep, cow, macaque, chimpanzee, and human,
the ability to reproduce is not in the large majority of cases synchronous with the appearance of the first
estrus or the menarche. The physiological prerequisites of reproduction are ovulation and the
maintenance of the developing fertilized egg within the uterus. Since these capacities do not generally
develop until some time after the advent of the first menstruation, conception and reproduction are,
therefore, in most cases, impossible during the menarcheal period. Before ovulation can take place the
endocrine system and the soma must reach a certain level of development. When that level of
development is attained ovulation occurs, and this is subsequently followed by the elaboration of
prolactin (luteotrophin), and finally of progesterone.

Hal. 209

The organism is then said to be nubile, the phase of development during which it first becomes viably
capable of conceiving and reproducing. Nubility and puberty are periods of development often confused
with one another, but in reality they represent two very different developmental processes.

The interval from menarche (which is only one expression of puberty) to nubility is termed the
adolescent sterility period, the period of adolescence during which the organism continues functionally
to be reproductively sterile. Obviously, this period is not, because of its sterile character, overtly
distinguishable from any of the preceding periods of development. It is here merely termed the
adolescent sterility period in view of the necessity of emphasizing what appears to be the fact that
menarche and the power to procreate are not synchronous events, but that the arrival of the one is
usually separated from the development of the other by an appreciable interval of time during which
the organism continues to be functionally sterile. This is not generally recognized to be the case.
Menarche is most commonly believed to be the sign of the development of the capacity to reproduce,
and the only interval at all recognized is that between menarche and maturity, the end of the period of
adolescence.

Maturity is generally taken to be the period that commences at the time when the growth of the
organism comes to an end, in humans at about 21 ± 2 years. This view, the evidence indicates, does not
appear to be sound. The period of adolescence is arbitrarily taken to begin at menarche, but the power
to procreate follows only at some time after this physiological function has developed. This is the period
of ovarian maturation when ovulation becomes possible and when conception may follow, the period of
nubility. This period, that is, nubility, is not coincident with maturity but represents the bridge, as it
were, between puberty and maturity; maturity being attained only at an appreciable time after the
development of nubility. The period of nubility is not by any means the best time for procreation, for it is
a period still characterized by high maternal and infant mortality rates.1

Hal. 210

The best time for reproduction is unquestionably at the age of early maturity, when the female
organism is fully prepared to undertake and carry through the processes of reproduction satisfactorily.

The physiological basis for the period of adolescent sterility is clear. It exists because the endocrine
glands, which must pour their hormones into the blood stream in the necessary concentrations before
ovulation and reproduction can occur, do not usually do so during the menarcheal or immediately
postmenarcheal period, but only during a later phase of development, the period of nubility.

The period of nubility marks the progress of another series of steps in the maturation of the sexual
equipment for the process of reproductive functioning. It does not by a long way represent the
completion of that maturation, but only the beginning. It is necessary to distinguish quite clearly
between the phases of puberty, nubility, and maturity.

Puberty may be defined as the period of the inception of those changes in the reproductive system that
are exhibited in the gradual development of the secondary sex characters and the appearance of the
first estrus or menarche. Physio¬ logically this means that the pituitary gland now releases the follicle
stimulating hormone (FSH) in increasingly greater concentrations, thus serving to produce secondary
sexual differentiation. FSH causes rapid growth of the follicle, the central cavity of which fills with
follicular fluid, which contains the hormones called estrogens. At this pre menarcheal phase of
development there is a sudden increase by some 40 percent in the FSH level. This high concentration of
FSH now acts upon the genital tract in a specific manner and results in the appearance of the first estrus
or menarche, and in the further development of the secondary sexual characters. During this and the
immediately continuing phase of puberal development the organism is normally sterile.

To state this in somewhat greater detail:

The three hormones of the anterior pituitary involved in reproductive function, are (1) FSH which
stimulates follicular growth to the preantral stage,

Hal. 211
(2) LH which initiates ovulation in the presence of prepared follicles, and

(3) prolactin, which stimulates milk secretion by the breast, and the maintenance of the morphologic
integrity and secretion of the corpora lutea. The two major glands of sex hormone secretion in the
human female ovary are the theca interna of the follicle, which secretes estradiol, and the luteinized
granulosa of the corpus luteum, which secretes progesterone.

The rising level of estradiol in the premenarcheal period initiates development of the secondary sexual
characteristics, the uterus, vagina, pubic hair, and about a year before menarche pigmentation of the
nipples and areolae, growth of the labia minora, and fat deposit in the labia majora. It is these changes,
and not menarche, which really announce the advent of puberty—a term which in its very origin means
the period of the appearance of hair on the pubes. A slight increase in the concentration of estradiol
during this period triggers the release of gonadotropin releasing factor (GRF) from the hypothalamus,
whereupon a surge of FSH from the anterior pituitary accompanied by a small amount of luteinizing
hormone, together known as folliculotropin, induces growth of the follicle and the secretion by its theca
interna of estrogen. With the development of a sufficiently high concentration of estrogen, probably
also secreted by the granulosa cells of the follicle, a fall in estrogen level is followed by endometrial
desquamation, a proliferative uterine endometrium is produced, and this results in the first
menstruation menarche. Repetition of these events results in subsequent menstrual cycles. In the
human female early menstrual cycles are especially liable to be anovulatory, but there is a great deal of
variability. On average, in the human female the anovulatory cycles last about three years.

The changes we have described that are initiated during puberty, after the lapse of a variable period of
time, are followed by a unique development, namely, ovulation. This marks the commencement of the
period of nubility. Nubility may be defined as that period of development during which the functions of
ovulation and reproductive potentiality are established in the organism.

Hal. 212

The duration of the sterility period in mouse, monkey, chimpanzee, and human, would appear to be
respectively one month, one to twelve months, four months to more than two years, and one month to
seven years. Variability in respect of the duration of this period is, of course, the rule, but the precise
limits of this variability in any of these groups remain to be determined. Nonetheless, it is clear that in
the chimpanzee and in man this variability is appreciable.
THE ITALICIZED HORMONES ORIGINATE IN THE PITUITARY GLAND

Adolescent sterility period Puberty 1. FSH increases by 40

13-16 ± 1 year percent
2. Follicular growth
3. First estrus or menarche
4. Anovulatory cycles
Nubility Nubility 1. FSH + LH
17-22 ± 2 years 2. Ovulation
3. Corpus luteum
4. Estrogen
Maturity Maturity 1. FSH + LH
23-28 ± 2 years 2. Ovulation
3. Estrogen
4. Prolactin (Luteotropin)
5. Corpus luteum
6. Progesterone

In about 25 percent of mice conception is possible at first estrus. In another study, it has been shown
that in some macaques conception is possible at first estrus, and that depending upon the state of
health of the animal the sterile period of the macaque may be but one month or it may be more than a
year. In humans the observations of gynecologists and anthropologists would indicate that the interval
between menarche and nubility is, on the whole, extremely variable.

The principal physiological changes characterizing the three main periods of reproductive development
in the human female are briefly resumed in Figure 8.

Hal. 213

Certainly, in the human species conception is possible at and even before menarche, and in many such
cases the fetus may be carried uneventfully to term, but these are proportionately the exceptional
cases. The adolescent sterility period is not one during which conception is impossible. Conception may
occur, generally it does not. When it does occur during the adolescent sterility period the reproductive
history of the individuals involved is generally marked by complications of pregnancy and a high infant
mortality rate.

Physiologically the period of nubility is characterized by the following events:

The rising concentrations of estradiol in the postmenarcheal female trigger the luteinizing releasing
hormone factor (LRF) which results in the release of luteinizing hormone from the hypothalamus. LH
acts synergistically with FSH to cause rapid swelling of the follicle which then re¬ leases an ovum
through the ovarian wall. The ovum is then taken up by the fimbria and passed into the uterine tube.
The follicular cells that previously surrounded the ovum, be¬ come luteinized, that is, they become
greatly enlarged and develop lipid inclusions that give the cells their distinctive yellow color, after which
fact the secretory body they form in the wall of the ovary, the corpus luteum, is named. The corpus
luteum produces most ofthe estrogen after ovulation under the stimulation mainly of LH.

Organization of the corpus luteum, and its maintenance as a temporary endocrine gland with its own
secretions is not, however, achieved till the development of the third gonadotropic hormone, namely
prolactin or luteotropin. It is the reorganizing action by prolactin of the corpus luteum that causes its
granulosa cells to secrete progesterone. It is progesterone that prepares the uterus for pregnancy, and
plays a role in preparing the breast (together with estrogens, corticosteroids, and growth hormone) for
lactation.

It is not until this third stage, that secretion of prolactin by the anterior pituitary and the action of this
upon the secretory functions of the corpus luteum to produce progesterone, that successful pregnancy
becomes possible.

Hal. 214

It is with the secretion of prolactin and progesterone that the period of reproductive maturity is
initiated, a period which remains at its optimum for about five years. The evidence we have surveyed
indicates that there exists an absolute period of adolescent sterility in most females during which
reproduction cannot occur. This period, among females of any given population, is extremely variable in
duration.

That a period of adolescent sterility normally exists in most human females is a fact substantiated as
much by the observed phenomenon as by the nature of the physiological processes involved in the
maturation of the reproductive system. This evidence strongly suggests that during early adolescence
the organism must, in most cases, necessarily be sterile.

The fact that the existence of such a period of infertility in the post puberal adolescent female has
escaped the attention of most human beings is not as difficult to understand as may at first appear. Nor
is it difficult to surmise how the belief came into being that the first menstruation represents a sign of
the female's arrival at the procreative stage of development. What seems most probable is that it had
been independently noted in various human groups that women remained sterile as long as they had
not menstruated, that after the first menstruation women menstruated periodically, and that during
their menstrual life alone were they capable of bearing children; for after the final cessation of these
periods (menopause) they were again sterile. Women capable of menstruation were therefore
considered to be capable of childbearing. Hence, the appearance of menstruation was taken to be the
sign of the ability to procreate.

The inference is certainly a logical one, but it is not wholly in accordance with the facts, and unless the
conditions are such as to make the observation a simple matter there is no possible way in which the
falsifying factors entering into this inference would become apparent to sense. Since these conditions
do not exist in most human societies it is practically universally believed that the first menstruation is a
sign of the ability to procreate. It has been shown, in these pages, that there is good reason to believe
that this is not the case.

Hal. 215

The fact that in almost all nonliterate societies the female is married immediately after she attains
menarche renders possible a sexual history for the person very different and much less trying than that
which the person experiences in literate societies. In nonliterate societies premarital intercourse is
usually, though not always, permitted. Since there is rarely any danger of pregnancy occurring before
menarche the problem of illegitimate children does not arise. On the other hand, cultures in which
marriage is postponed till some years after menarche, that is, until the postmenarchial nubile period,
cannot permit premarital inter¬ course owing to the fact that the birth of many children out of wedlock
would have a socially disrupting effect—for undoubtedly many of them would be born during the
menarche-nubility interval. Hence, this additional impediment in such societies toward the recognition
of an adolescent sterility interval.

We now come to the final practical conclusion of this study, namely, that the best time for conception,
pregnancy, and childbirth in the human female is, on the average, at the age of 23 ± 2 years and for
about five years thereafter. The society that would be healthy would do well to consider these facts, and
would encourage the awareness of their significance for the female accordingly.

Hal. 216