Testosterone
Propionate Treatment of an XY Gonadal Dysgenetic
Chacma Baboon
C. Bielert
Primate Behaviour Research
Group, School of Psychology, University of the
Witwaters rand, Johannesburg, South
Africa
Behavioral studies of an XY gonadal
dysgenetic chacma baboon prior to and during
testosterone propionate treatment were carried
out. The orchidectomized dysgenetic individual,
two intact males, a castrate male, and two
ovariectomized females were pair-tested with a
group of eight ovariectomized stimulus females
prior to and during their treatment with
estradiol benzoate. Three test series were
carried out. One series occurred prior to any
treatment of the agonadal focal subject animals.
During this series it was only the intact males
who showed behavior change during their testing
with the estrogen treated females. A second test
series occurred after a month of daily
testosterone propionate injections (I mg/kg/day)
had been given to the four agonadal subjects.
During this test series the castrate male
ejaculated once with one of the estrogen-treated
females. All of the treated subjects showed
increases in their frequency of yawning. Upon
completion of this test series the androgen
dosage was increased (2 mg/kg/day) and 2 weeks
later a third test series was carried out.
During this series the castrate male ejaculated
with five of his eight estrogen-treated
partners. The yawning of all the treated
subjects continued. As had been the case in the
second series the XY gonadal dysgenetic
individual continued to behave as did the
ovariectomized females. None of these animals
showed any increase in any measure of male
sexual behavior. This study establishes the fact
that a genetic male primate deprived of in utero
exposure to testicular hormones will go on to
develop as a normal genetic female and will fail
to exhibit increased levels of male sexual
behavior during androgen treatment.
The general proposition that 'gonadal
hormones secreted prenatally act on the
developing brain so that the individual behaves
predominantly as a male or female in adulthood"
has been stated (Goy, 1968: p. 12). It has been
pointed out that recent work (Bielert, 1984a,b)
with an adult XY gonadal dysgenetic chacma
baboon (Papio ursinus) allows for a critical
examination of the view that a genetic male in
the absence of appropriate early testicular
activity will go on to develop as a normal
female.
The dysgenetic individual, Que sta, presents
phenotypically as a female. The animal is large
but eunuchoid in development. Her size is
consistent with her genetic disorder (Madan and
Schoemaker, 1980) but somewhat inconsistent with
her phenotype. Upon initial housing Questa
weighed 27.4 kg (A" ± SD for eight adult
males upon initial housing 24.6 ± 4,1 kg
and 18.0 ± 1.9 kg for eight adult females).
Questa was wild caught as an adult and she has
been individually caged and unmanipulated except
for previous experimental work assessing her
behavior. There is no reason to believe that her
socialization in the wild would have been in any
way deficient. Her troop membership is ample
proof of her acceptance by conspecifics.
An initial study made it clear that the
dysgenetic individual, Questa, was treated as a
female by conspecific adult males and that
female conspecifics also reacted to this
individual as they do to other adult females
(Bielert, 1984a). In other words this individual
was treated by others in a fashion consistent
with her phenotype with no real evidence that
her genotype affected the way others reacted to
her in spite of her unusual size.
The next study in which she was involved was
an assessment of the reaction of Questa to
estradiol benzoate therapy (Bielert, 1984b). The
results of this study made it clear that with
appropriate estradiol treatment Questa behaves
as a normal genetic female.
The question of Questa's reaction to
androgen is an important one to address. The
prediction would be that Questa should not show
the sort of reaction to testosterone that could
be expected as an example from a castrated adult
genetic male. This is a consequence of the fact
that early testicular hormone exposure
"organizes" masculine behavior patterns and
Questa should not have had such exposure and so
should not react in a sex-typical fashion.
Although recently the applicability of the
organizational hypothesis in terms of human
sexual expression has been critically questioned
(Feder, 1984), the applicability of this
hypothesis in the case of nonhuman primates and
their sexual behavior is more apparent. Data
collected from nonhuman primates is important
for it allows for speculation about the human
situation and offers the opportunity of
controlled and ethical experimentation. Although
one can always question the appropriateness of
laboratory pair tests as a testing paradigm it
would appear that the basic data collected in
such a fashion would still have extensibility in
a more complex social setting such as the wild
even if there were a number of new variables
which might also exert their effects in such a
situation.
DISCUSSION
The results of this study are consistent
with the view that a genetic male nonhuman
primate when deprived of appropriate gonadal
activity in utero will proceed to develop along
the lines of a typical genetic female. It has
already been pointed out (Bielert et al., 1980b)
that Questa's anatomic development was typical
of that of a genetic female. Previous work has
shown that she is treated as a female by both
unfamiliar male and unfamiliar female
conspecifics (Bielert, 1984a). In addition it is
clear that she responds to estradiol benzoate
treatment in a fashion typical of a normal
genetic female (Bielert, 1984b). The contrast
which existed between the castrate male and
Questa in regard to the effectiveness of the
androgen therapy suggests that it is only
genetic males who have received in utero gonadal
hormone exposure who will later show a response
to androgen stimulation.
It could be argued that for some reason or
other Questa was "insensitive" to the androgen,
in other words that the lack of response was due
to something other than her response potential.
The data on weight gain make it clear that she
shows a typical anabolic response to
testosterone. It is impossible to speculate on
whether in this regard Questa gave evidence of a
"masculine" rather than a "feminine" response
but the similarity between the castrate male and
Questa is intriguing. Questa along with the
castrate male and the ovariectomized females
responded to the androgen therapy with an
increase in yawning consistent with that which
has been previously observed in macaques (Eaton,
Goy, and Phoenix, 1973; Goy and Resko, 1972;
Phoenix and Chambers, 1982). It should be added
here that Questa's yawning level during androgen
treatment was more similar to that of the
ovariectornized females than to that of the
castrate male. Again, however, it is impossible
to determine whether this may reflect some
neuroendocrine bias or not since our subject
sample size was so small. Taken together
Questa's weight gain and yawning increase
suggest that there were no problems of
bioavailability of testosterone propionate in
reaching target structures.
In terms of the overall trends apparent in
the data Questa behaved as a genetic female
receiving androgen therapy and not as a genetic
male receiving this same treatment. It is
possible to say that in essence negative results
are being reported. In at least one study
(Bielert, 1974) prepubertally castrated male
rhesus monkeys (Macaca inula (ta) when androgen
treated in adulthood failed to exhibit
consummatory sexual responses. The importance of
rearing conditions in determining sexual
performance has been appropriately stressed in
the case of the captive primate (Goldfoot, 1977)
and at the moment it seems premature to suggest
prepubertal castration necessarily mitigates
against the later display of complete mating
behavior under appropriate hormone therapy. I
firmly feel that the results of the present
study should be viewed as consistent with others
that have been previously obtained in terms of
the ineffectiveness of androgen therapy in the
stimulation of male sexual behavior in normal
genetic female primates Eaton et al., 1973;
Phoenix and Chambers, 1982). This is so even at
the very reduced assessment level of contacting
behavior which genetic females are totally
capable of exhibiting (refer to Table 1).
The number of experimental behavioral
studies with primates relevant to the
organization hypothesis of early gonadal
hormonal action on adult sexually dimorphe
behavior patterns is small. Work has been
carried out with marmosets (Callithrixjacchus)
(Abbott and Hearn, 1979), rhesus macaques (M.
mulatta) (Goy and Resko, 1972; Eaton, Goy, and
Resko, 1973; Goy, Wolf, and Eisele, 1977; Goy,
1981; Phoenix and Chambers, 1982; Phoenix,
Jensen, and Chambers, 1983) and the chacma
baboon (P. ursinus) (Bielert, 1984a,b and the
present study). Thus far, however, there has
been no good evidence on which to reject the
view that exposure to early gonadal hormones or
an exogenous androgen during the "critical
period" for sexual differentiation of the brain
results in a shift toward the masculine and of
the behavioral spectrum. The results of the
present study when considered along with those
previously obtained (Bielert, 1984b) make it
clear that a genetic male nonhuman primate when
deprived of appropriate testicular hormone
exposure develops along the lines of a genetic
female and it is clear that genetic female
primates do not show any increase in their
display of male sexual behavior with androgen
treatment (Eaton, Goy, and Phoenix, 1973;
Phoenix and Chambers, 1982; and the present
study). These facts taken together give the
organizational hypothesis some fairly
substantive support. The question of the
applicability of this hypothesis to the human
species is a somewhat nagging one. It is the
question of adult sexual behavior which,
although the most studied behavior pattern by
workers experimenting with animals and examining
the organizational hypothesis, has raised the
most doubts about the extension of this
hypothesis to humans. Human sexual behavior is
much more varied in its expression, hormonal
control, and social modulation than that of any
other primate. Perhaps it is expecting too much
if one expects to find the same sort of sexual
behavior dimorphisms in humans as encountered in
other species. It may well be that the
continuity between humans and animals comes at a
different level of comparison. It would appear
that there are species differences in the
potential bisexuality of a particular genetic
sex (Goy and Goldfoot, 1973) and from the small
amount of data available it would appear that
normal male primates have a greater potentiality
for the display of dimorphic sexual behavior
patterns typical of females than vice-versa. If
this can be accepted as the case then the
presented results from Questa suggest that this
variability may result from early hormonal
exposure. If this variability is relevant to the
sexual display of adult humans then it is
perhaps appropriate to look for valid
cross-cultural sex differences in the nature of
sexual interactions among male-male,
male-female, and female-female pairs of humans.
One might expect to find differences between the
sexes in terms of the proportions with which a
specific sex exhibits a particular sexual
behavior pattern more typically shown by the
opposite sex. The small amount of data which
exists on sexual dimorphism in the human central
nervous system (Baack et al., 1982; De
Lacoste-Utamsing and Holloway, 1982) may be
supportive of a sex difference in cognitive
abilities and it is this cognitive level which
may interact with an organized plasticity in
dimorphic sexual behavior display and express
itself in the typical and atypical sexual
behavior patterns of the human male. If this
reported primate example has relevance for the
human situation it would be to suggest that in
the absence of appropriate fetal hormone
exposure a genetic male is totally capable of
full operation as a typical genetic female who
will therefore not exhibit increases in male
sexual behavior as a consequence of androgen
stimulation.
«
It is ironic that testosterone "the male sex
hormone," is more closely associated with the
yawning rate than with the mounting or
intromitting rates » Charles
Phoenix
Sexual
steroids
exert several effects on both central
dopaminergic and oxytocinergic systems by acting
either at the genomic or membrane level
