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1 mai 2010
Hormones and Behavior
 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.
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
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