Dihydrotestosterone
Propionate Effects on Dominance and Sexual
Behaviors in Gonadectomized Male and Female
Rhesus Monkeys
Cochran CA, Perachio AA
Laboratory of
Neurophysiology Yerkes Regional Primate Research
Center, Emory University, Atlanta,
Georgia
One triad of male and two triads of female
gonadectomized rhesus monkeys were observed as
social groups assembled for repeated hour-long
sessions. Social relationships were measured in
terms of aggressive behavior between the members
of each group in order to determine the
dominance hierarchical order. Sexual performance
was assessed for each male, before and alter
castration, in tests with an estrogen-stimulated
ovariectoinized female. Siniilar measures were
made when the same female was periodically
introduced to the all-male triad. When
dihydrotestosterone propionate (DHTP) was
administered for a period of 6 weeks to the
middle-ranking member of each group, social
status changes occurred in two groups, one male
and one female, resulting in the elevation of
the treated monkeys to the highest rank in the
dominance hierarchy. In the other female group,
aggressive behavior was increased with DHTP
treatment of the middle-ranking female. Somatic
effects, particularly again in body weight,
occurred in all treated animals. Yawning
behavior also increased significantly in those
animals receiving DHTP. The latter two effects
returned toward pretreatment levels following
the cessation of hormone injection; however,
changes in dominance hierarchy persisted to the
end of the experiment, 6 weeks following the
last DHTP treatment.
The role of gonadal hormones in the
regulation of social behavior has been evaluated
in nonhuman primates through measures of
aggressive interactions and sexual behavior.
Treatment with testosterone can increase
aggression and alter dominance status in infant
female rhesus monkeys (Joslyn, 1973) and adult
female chimpanzees (Birch and Clark, 1946). In
social groups of talapoins, castrated males
treated with testosterone became more aggressive
toward lower ranking male members of a
heterosexual group, while not producing any
change in social hierarchy (Dixson and Herbert,
1974). Alternatively, it has been reported that
testosterone has no marked effect on the
aggressive behavior or social standing of
adolescent female or male rhesus monkeys
(Mirsky, 1955) and adult male or female squirrel
monkeys (Green, Whalen, Rutley, and Battie,
1972). With respect to sexual behavior,
testosterone propionate (TP) treatment can
restore the performance of castrated male
rhesus
monkeys to more or less preoperative levels
(Phoenix, 1973; Michael and Wilson, 1974).
Testosterone treatment of ovariectomized
estrogenprimed female rhesus monkeys has
elevated sexual behavior (Trimble and Herbert,
1968; Goy and Resko, 1972). Similarly,
androstenedione and testosterone have restored
sexual receptivity in adrenalectomized,
ovariectomized, estrogen-treated female rhesus
monkeys (Everitt, Herbert, and Hamer, 1972;
Everitt and Herbert, 1975).
A metabolite of testosterone,
dihydrotestosterone (5a-androstan- 17/3ol-3-one;
DHT), has been implicated as a possible factor
in the behavioral-endocrine mechanisms
underlying sexual behavior in male rhesus
monkeys (Phoenix, 1974). When administered to
long-term castrated males, DHT, in the
propionate form (DHTP), was found to restore
sexual performance as effectively as TP. These
findings stand in contrast to earlier work with
other species which demonstrated that DHT failed
to promote or maintain sexual behavior in
castrated male rats (McDonald, Beyer, Newton,
Brien, Baker, Tan, Sampson, Kitching, Greenhill,
and Pritchard, 1970; Whalen and Luttge, 1971)
and that it was less effective than TP in
initiating sexual behavior in prepuberally
castrated rabbits (Beyer and Rivaud, 1973).
Since DHT, unlike testosterone, is not
aromatized to estrogenic compounds, the
influence of this hormone on castrated male
rhesus sexual behavior implies an
androgen-related mechanism. In females, a
similar mechanism may be important for sexual
behavior. Although DHT has not been investigated
in rhesus females, the androgenic effects of
testosterone and its metabolites may account for
the restoration of sexual receptivity in
adrenalectomized females following treatment
with hypothalamic implants of TP (Everitt and
Herbert, 1975).
If an androgenic hormone effect is a
necessary component of sexual and aggressive
behavior, a nonaromatizable androgen compound
such as DHT would be a useful investigative
tool. Given the apparent sensitivity of the
species to this hormone and the equivocal
results obtained with testosterone treatment in
producing changes in dominance and aggression, a
set of experiments was designed to investigate
the effects of DHT on social dominance in
gonadectomized male and female rhesus monkeys as
reflected in measures of sexual and agonistic
behaviors.
DISCUSSION
The results of this experiment indicate that
DHT can influence social interactions in
gonadectomized adult male and female rhesus
monkeys, leading to a disruption of the social
structure of small groups and producing a
long-term alteration in the dominance hierarchy.
The present investigation also provides support
for previous findings (Phoenix, 1974) that DHTP
can restore sexual performance in long-term
castrated male rhesus monkeys. In addition to
physiological variables, aspects of the
experimental design, including group size,
gender of members of the group, acuteness of
social contact, and size of the observation
cage, may have contributed to this set of
findings. The DHTP effects on behavior may also
have been species-dependent. Peripheral tissue
responses during hormone treatment, as reflected
by weight gain and reddening of sex skin in the
treated monkeys, resembled those reported for
nonprimate species; however, the effects of DHT
on some behavioral measures in this experiment,
e.g., restoration of the castrated male's sexual
behavior, differed from those reported for some
nonprimates (McDonald et al., 1970; Whalen and
Luttge, 1971; Beyer and Rivaud, 1973).
Previous investigations failed to detect
changes in primate dominance hierarchies with
androgen treatment (Mirsky, 1955; Green et al.,
1972). In part, this may have been due to the
use of testosterone as the treatment hormone.
However, other factors distinguish those studies
from the present experiment. On one hand, the
social rank of the treated animal may mask the
social consequences of behavior affected by the
hormone. In one study (Green et al., 1972),
testosterone was administered only to the two
highest ranking members of two groups, each
composed of six squirrel monkeys; thus, any
possible change in social status was limited.
However, in another experiment (Mirsky, 1955),
TP was given first to the lowest and then to the
second-ranking members of two groups of five
rhesus monkeys; no dominance alteration was
noted. Alternatively, the social conditions in
those tests may have been a crucial variable. In
both studies (Mirsky, 1955; Green et al., 1972),
the monkeys were housed and tested together
throughout the experiment; in the present
investigation, the animals were housed
individually between test sessions. Acute social
contact may exacerbate hormonal effects on
behavior. This notion is reinforced by the
incidental observation that, in most groups in
our experiment, more intense aggression was
exhibited in the early portion of each test.
Further evidence that duration of social contact
is important is
DISCUSSION
The results of this experiment indicate that
DHT can influence social interactions in
gonadectomized adult male and female rhesus
monkeys, leading to a disruption of the social
structure of small groups and producing a
long-term alteration in the dominance hierarchy.
The present investigation also provides support
for previous findings (Phoenix, 1974) that DHTP
can restore sexual performance in long-term
castrated male rhesus monkeys. In addition to
physiological variables, aspects of the
experimental design, including group size,
gender of members of the group, acuteness of
social contact, and size of the observation
cage, may have contributed to this set of
findings. The DHTP effects on behavior may also
have been species-dependent. Peripheral tissue
responses during hormone treatment, as reflected
by weight gain and reddening of sex skin in the
treated monkeys, resembled those reported for
nonprimate species; however, the effects of DHT
on some behavioral measures in this experiment,
e.g., restoration of the castrated male's sexual
behavior, differed from those reported for some
nonprimates (McDonald et al., 1970; Whalen and
Luttge, 1971; Beyer and Rivaud, 1973).
Previous investigations failed to detect
changes in primate dominance hierarchies with
androgen treatment (Mirsky, 1955; Green et al.,
1972). In part, this may have been due to the
use of testosterone as the treatment hormone.
However, other factors distinguish those studies
from the present experiment. On one hand, the
social rank of the treated animal may mask the
social consequences of behavior affected by the
hormone. In one study (Green et al., 1972),
testosterone was administered only to the two
highest ranking members of two groups, each
composed of six squirrel monkeys; thus, any
possible change in social status was limited.
However, in another experiment (Mirsky, 1955),
TP was given first to the lowest and then to the
second-ranking members of two groups of five
rhesus monkeys; no dominance alteration was
noted. Alternatively, the social conditions in
those tests may have been a crucial variable. In
both studies (Mirsky, 1955; Green et al., 1972),
the monkeys were housed and tested together
throughout the experiment; in the present
investigation, the animals were housed
individually between test sessions. Acute social
contact may exacerbate hormonal effects on
behavior. This notion is reinforced by the
incidental observation that, in most groups in
our experiment, more intense aggression was
exhibited in the early portion of each test.
Further evidence that duration of social contact
is important is the fact that Female Group I, in
which a dominance reversal did not take place,
had been established for a longer period than
had the other groups. The amount of time the
animals spent together seems to have affected
the stability of the group.
Not all effects observed can be readily
ascribed to a physiological mechanism affected
by the hormone treatments. The increases in limb
shaking displays may have been a type of
indirect effect of DHTP treatment. This
behavior, also referred to as cage or branch
shaking, is typical of dominant rhesus monkeys
and is rarely seen in a subordinate animal
(Altmann, 1962). During DHTP treatment, limb
shaking behavior was displayed more often by the
dominant animals in all groups. Since this
included the untreated dominant female in the
group that did not alter its dominance
hierarchy, the change in behavior was not
related to a physiological effect of DHTP.
In contrast, yawning displays, typical of
adult male rhesus monkeys in stressful
situations, appeared to be more directly related
to the hormone treatment. It has previously been
found that TP increases the frequency of yawning
in adult rhesus females in a social group
context (Goy and Resko, 1972; Phoenix, 1973).
Similarly, an increase in yawning was observed
with DHTP treatment of castrated male rhesus
monkeys (Phoenix, 1974). Yawning in the
DHTP-treated animals occurred independently of
changes in their dominance rank; however, it
seemed to be related to social variables, since
the frequency of this behavior was noticeably
increased when the treated animals joined their
respective groups for test sessions. Somatic
changes were another example of physiological
effects of DHT that were apparently unrelated to
behavioral variables. A gain in weight was
measured in all the treated subjects, including
the female (NP 42) whose dominance standing was
unaltered.
Although the results reaffirm earlier
findings that DHT can effectively restore sexual
behavior in castrated male rhesus monkeys
(Phoenix, 1974), we are unable to state whether
this hormone affects female receptivity, since
pair tests were not used with the female groups.
Sexual behavior in the triads was confounded
with variables related to the social
relationship between group members. In any
event, the lack of noticeable alteration in
female rhesus sexual behavior following
administration of DHT is consistent with similar
findings in female rats and rabbits (Beyer,
McDonald, and VidaI, 1970; Beyer, Morali, and
Cruz, 1971).
The importance of DHT per se for the
regulation of sexual or aggressive behavior in
rhesus monkeys remains in question. For example,
no direct relationship has been found between
plasma levels of DHT (or testosterone) and male
rhesus monkey sexual behavior (Robinson,
Scheffler, Eisele, and Goy, 1975). However,
given the qualifications just discussed, our
data indicate that an androgen-related mechanism
is relevant to the endocrine basis of social
aggression in both male and female rhesus
monkeys. This conclusion must be further
tempered by the caution that should attend the
interpretation of the behavioral effects
produced by pharmacological hormone dosages
administered as replacement treatment in
gonadectomized animals. At present, we propose
that further investigation of the hormonal
relationships to behavior should consider
androgenic compounds, including DHT, as
mediators of aggressive behavior, which, in
unstable social groups, can promote alterations
in group social structure.
«
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
