You are on page 1of 13


/988, Vol. /6 (4), 335-347

Sex hormones and sexual orientation in animals
Cornell University, Ithaca, New York

This review critically examines whether sex hormone exposure during prenatal or early post-
natal development determines the adult sexual orientation (sexual preferences) of animals. In
rats, hamsters, ferrets, pigs, zebra finches, and possibly dogs, either early castration of males
or early testosterone treatment offemales or both have been shown to change or reverse sexual
orientation. The effects of early sex hormone exposure on copulatory behavior, studies of prena-
tal hormones and sexual orientation in humans, different animal models for research on sexual
orientation, and the desirability of a broad psychobiological investigation of sexual orientation
in animals are discussed.

Tbe influence of sex hormone exposure during prenatal sexual orientation in nonhuman animals. Is this the case?
or early postnatal development on the sexual orientation Most positive claims eite inappropriate experiments, in-
of animals would seem to be an obvious topic for research, dicating a need for a more critical review of the relevant
yet this subject has received surprisingly little attention. animal literature.
Since the publication of Young, Goy, and Phoenix's
(1964) influential paper outlining an organizational the- TERMINOLOGICAL AND
ory of behavioral sexual differentiation, a great deal has CONCEPTUALISSUES
been learned about how sex hormones produced during
the neonatal period determine sex differences in copula- Nonhuman animals (hereafter called simply animals),
tory behavior, but much less attention has been given to like most humans, show consistent courtship and mating
the possibility that these early hormones might influence preferences for either males or females. I will use the
not only how frequently animals copulate or what motor terms sexual preferences and sexual orientation nearly
pattern they exhibit in a sexual interaction, but also which interchangeably to refer to this phenomenon, although in
sex they choose to spend sexual time with. In the past few the ethology literature the term sexual preference is gener-
years, however, there has begun to be a significant body ally associated with experiments on animals ' mating
of work on early sex hormones and sexual orientation in preferences for one species or color form versus another
animals. (e.g., Bateson, 1978). What is critical in determining an
A review of this literature is timely because of increas- animal's sexual orientation/preference is that the subject
ing interest in the possibility that human variation in sex- be observed with stimulus animals of both sexes, prefer-
ual orientation has a prenatal sex hormone basis. Tbe most ably in some kind of choice situation. It is weH known
complete and explicit statement of the theory that prenatal that if animals are tested only with same-sex partners, they
hormone exposure determines who will be heterosexual, will copulate with them, particularly if the subjects are
homosexual, or transsexual has been made by Dörner sexually deprived or treated with heterologous sex hor-
(1976; see also Dörner, 1988, for a more recent sum- mones (ovarian hormones for males, testicular hormones
mary). Several studies of humans have been interpreted for females) (Adkins-Regan, 1981; Feder, 1981; Young,
as lending support to this theory (see reviews by EHis & 1961). But such observations do not necessarily mean that,
Ames, 1987; Meyer-Bahlburg, 1984; Money, 1987; and given a choice, they would prefer to interact sexually with
the report by Gladue, Green, & Hallman, 1984). There same-sex partners. Similarly, experiments measuring time
are many problems with these experiments that have al- spent by males with estrous versus nonestrous females or
ready been succinctly summarized (Baum, Carroll, Er- time spent with estrous females by intact versus castrated
skine, & Tobet, 1985; Gooren, 1984; Meyer-Bahlburg, males, although interesting for understanding sexual moti-
1984), and there have been difficulties with replication vation, are not relevant to the question as to whether early
(Gooren, 1986; Gooren, Rao, van Kessel, & Harmsen- sex hormones determine sexual orientation.
Louman, 1984). In addition, the human literature assumes Also, sexual orientation does not refer to the copula-
that early sex hormones have been shown to determine tory motor patterns that the animal performs. A male rat
mounting another male is engaging in a homosexual inter-
action, but a female rat mounting a male is not. She is
This work was supported by National Science Foundation Grants BNS-
showing male-typical (heterotypical) behavior, but is inter-
8204462 and INT-8603645 and by an American Fulbright Research Scho-
lar Award. Requests for reprints should be sent to Elizabeth Adkins- acting sexually with an opposite-sex, not same-sex, part-
Regan, Department of Psychology, 218 Uris Hall, Comell University, ner; she is engaging in a heterosexual, not homosexual,
Ithaca, NY 14853-7601. interaction.

335 Copyright 1988 Psychonomic Society, Inc.

they prefer to spend time with females. ment grow up to be female-like. 1981). effects that cause males to become more female-like.. that masculinization (increase in male-typical behavior) It is also important to distinguish between sexual prefer. 1976). appropriate (see Baum. as weU as some understanding of the roles ofthe sexes in mate choice. either males mate with more than one male. does the female normally do most of the choos- ing? Tbe male? Both? Experiments on rats are often cited in support of hor- Tbus. shock grids between the sub- ation occurs. they are often 1987). Gooren. Feder. including double- In the absence of testicular hormones. In or even estradiol (E) grow up to be male-like. are females and less time with males than do controls.g. probably lead to male differentiation by masculinizing behavior (in. choice runways or T-mazes. fe- McEwen. Gründ. rather than actual animals themselves. 1983a) actually female-typical are separate behavioral dimensions. treatments on sexual orientation (i. so that the measures would more accurately low levels of receptivity foUowing priming with E or E reflect appetitive/motivational aspects of mating prefer- . only two were sensitive to these important distinc.336 ADKlNS-REGAN The serious conceptual error committed by confusing plus progesterone (P).. Beach. Meyer-Bahlburg. 1978. male-typical and female-typical sexual preferences can lach. and arenas with tethered stimulus animals. In mammals. Because the vet. and feminization for and would reflect some knowledge of the social organi. experiments that are discussed grew out of research on rather than pronounced. both sexes choose mating partners. Tbe relative importance of masculinization versus several studies of the effects of different adult hormone deferninization in male development depends on the spe. Behavioral and physical dimorphism is slight. yet the error persists. 1968). and if there is any mate choice. In the species under RATS (Rattus norvegicus) study. or female-typical (Baum. For this reason. that are more than one female (McClintock. cies and on which type of copulatory behavior is more see below for specific references). as adults they show low havior when exposed only to same-sex partners has been levels of mounting foUowing prirning with T compared explained quite articulately several times (e. 1974. with controls and/or high levels of receptivity foHowing 1979. should not direct exarninations of sexual orientation. 1973). and time spent have no bearing on mating preferences. 1984. however. female differenti. Iftestosterone-treated females spend more time with versus females. early hormone influences in animals that are supposedly Studies of organizational effects of sex hormones on relevant to a "neurohormonal" theory of human copulatory behavior have established that male-typical and homosexuality. Meyer-Bahlburg. arenas with stimulus animals for female behavioral development. Males castrated early in develop- sexual orientation with the capacity for heterotypical be. referred to as "organizational" effects. such females rnight weH also vary independently. abrief and is unknown. like most mammals. as opposed to the tions (Gooren. 1984. and if the right experimental measure is used. travel together and interact with males In theory. experi. 1988. this review focuses on experiments that actually monal theories of human sexual orientation. Offive re. only during the breeding season (Frädrich. These sex-reversing effects cent reviews of the prenatal hormone hypothesis of hu. with one sex is time that cannot be spent with the other ments in which the stimuli are odors taken from males sex. and types of apparatus have been used. of early gonadal hormone manipulations are permanent man sexual orientation (Dörner. Money. but. females to become more male-like. compared some of the experiments. In choice tests. 1979). the adult females show allowed to have fuU physical contact with or to mate with high levels of mounting foHowing prirning with T and/or the stimuli. they are unlikely somewhat oversimplified summary of this process is to be monogamous or to form pair bonds (Kleiman. in wire-mesh cages either inside or positioned around the males treated early in development with testosterone (T) outside. thus the ovaries do not seem to be critical ject and the stimulus animal. activational effects. zation of the species. can occur independently of deferninization (decrease in ences and nonsexual social preferences. Meyerson & Lindström. fe. creasing the capacity for male-typical behavior such as Tbere have been two extensive investigations ofthe sex- mounting) or deferninizing behavior (decreasing the ca. but such results would cannot. EHis and temporary "activational" effects of sex hormones ad- Ames (1987) cited nearly 40 published experiments on rninistered in adulthood. will use the term masculinization for any effect that causes sure that the primary motivation for the choice is sexual. 1987). Experimentally. for example. Davidson. A variety of methods dimorphic. the subjects were not actually with neonatally untreated controls. Both sexes produced during prenatal or early postnatal development actively court. as weH as both. Goy & When domestic rats are observed mating in groups. In most studies. EUis & Ames. male-typical. The ideal the effect be called masculinization or deferninization? I sexual preference experiment would be designed to en. and males mate with androgens or estrogens derived from androgens. pigs. neonatal development. 1977). and measured sexual orientation.e. Tbe mating system of wild rats sexual differentiation of copulatory behavior. 1981. ual preferences of normal intact adult rats (Hetta & Meyer- pacity for female-typical behavior such as lordosis) or son. and are usually possible only during a critical period in 1987. 1979. 1984). testicular hormones. 1980). 1979). because tests are fixed in length. Only one ofthese (Ford. Adult female wild female-typical behavior). 1984. and vice versa (Feder. prirning with E or E plus P. way rats live and reproduce in groups (Robataille & Bou- uations involving male and female stimuli. Wild Nor- deterrnined sexually motivated preferences in choice sit. Sirnilarly.

received estrogen priming plus third ventricle infusion of Meyerson. activational and (Dudley & Moss. and some were given TP on Days 2 tation of female rats. 1986.g estradiol benzoate (EB) used a circular arena with a box containing a sexually ac- three times per week (a 20:1 ratio ofTP:EB). TP as adults. but castrated males tested at 70 days also preferred the fe- failed to activate lordosis.or TP-treated females given An experiment by de Jonge. Stimulus tion between sexual experience and mate choice in females animals were sexually active intact males or ovariec. Testing began at 100 days. Overdijk. In another experiment. status of the rat at the time of testing. only compared the sexual preferences of experienced versus those that had received TP on Days 2 and 4 preferred fe- naive females ovariectomized as adults and given oil or males (Figure 1). The preference of males for estrous fe- males prefer estrous females over males (Hetta & Meyer. TP-treated females did show a preference for males. The greater effectiveness of P in replacement. Hetta & adult sex steroid treatments on the sexual orientation of Meyerson. which cannot be converted to estrogen. perience. Naive females receiving oil showed no preferences. Slob et al. and van de Poll (1986). Slob. & Brand. the preference of Thus. Less is known about the hormonal basis of male rat sex- Intact females prefer males over females. using doses of TP Eliasson and Meyerson (1981) studied intact males and and EB matched for activation of lordosis (1 p. males were castrated ways with sexual experience to determine the sexual orien. & Dissinger. but significantly less so. (1987) experiment. LHRH of neonatal sex hormones in both sexes. that the synthetic an. In contrast. Testing began at 200 days. and time spent with the male decreased. is not sufficient to conclude that Ileonatal testicular hor- tivity (hopping and darting) but not preference for males. Eerland. and intact ual orientation. females were given TP at 5 days of age or were males in a choice apparatus.or TP. interaction between experience and hormones. Meyerson & Lindström. the intact males single injection. and the de Poll. & van hormones in the expression ofthese preferences. With de Jonge. Loeb. But females this feminization is expressed only following adult EB. Eliasson. Female sex. It and van de Poll (1988) compared the sexual orientation will be important for researchers to look at the interac. preferences are mediated in part by odors and the olfac- Three experiments compared the effects of different tory system (Carr. and Hetta (1980) examined the role luteinizing hormone releasing hormone (LHRH). the females showed no preferences. ANIMAL SEXUAL ORlENTATION 337 ence unconfounded by consummatory aspects. then with TP replace- after being allowed to interact with a freely moving male. (1987) found about the sexual differentiation ofthese preferences. however. and that P given to EB. 24-36 h after birth. De Jonge. mones influence sexual orientation in rats. subjects were tested 500 p. 1965. male. Louwerse. Muntjewerff. Without hormone the Dudley and Moss (1985) experiment than in the replacement. males over males occurs even without prior sexual ex- son. and females were tested without hormone in the same apparatus. The neonatally readily stimulated the preference for males as well. With TP in adulthood. This preference in- creasing the preference for males. adult ovariectomized females. However. sexual experience with males showed no preferences. the role of adult activational increased by injection with E (de Jonge. Meyerson & Lindström. and fi- they switched to a preference for females. 1985) in which ovariectomized females organizational hormone actions were confounded. Eerland. These results TP. but with EB in adulthood. and 4 while others were not. oil. untreated. nally with EB. 1987).g EB and males castrated within 24 h ofbirth. van Haaren. At 30 days. In the Slob et al. These de Klerk.g TP. drogen R1881. male injected with E plus P. in spite ofthe fact that P fol. that is. the others preferred males. the neonatally androgenized probably due to the 25-fold greater dosage used. then again with no hormone replacement. and van de Poll (1986) and de Jonge. and van de Poll (1987) males preferred females. or with TP. with mount experience (experience with females) TP can make up for the neonatal absence of testes. Kalverdijk. 3-4 weeks after 10wing estrogen priming did increase preference for males ovariectomy. they preferred males. and is reduced by castration and increased by ual preferences are determined in part by the hormonal injection with T (Hetta & Meyerson. 1973). because the These results suggest that the mechanisms for sexual two groups were different hormonally at the time of test- preference and for receptivity/proceptivity are different. of female rats injected with TP within 24 h of birth with . both groups of Burger. 1978).4 mg testosterone propionate three studies have looked at the effect of neonatal hor- (TP) three times per week showed weaker preferences for mone manipulations on adult sexual orientation. found that TP was more effective for in. 1978). This experiment by itself primed females facilitated both receptivity and procep. 1973. and preferred females. but when treated with TP. 1978. and van de Poll (1986) experiment is either EB or TP in adulthood. time spent with the female increased. there is good background information about the females for stimulus males is reduced by ovariectomy and sexual preferences of rats. tive male versus a box containing an ovariectomized fe- de Jonge. females preferred stimulus females instead of males The adult hormone environment interacts in important (Figure 1). show that neonatally castrated males are feminized. tomized females brought into heat with E plus P. receiving homologous hormones (E plus P) as adults. already slightly preferred the female. ing as weH as neonatally (neonatally castrated males did Such a dissociation is also indicated by an experiment not receive hormone replacement). All three males than females given 20 p. with EB. creased with age. Remarkably little is known. In one experi- enhanced receptivity but did not increase preference for ment. but first with no hormone replacement. regardless of whether they received early TP masculinizes females. ment. Eerland. a 500: 1 ratio of TP: EB) and giving only a from 30 to 120 days of age. Only that females injected with 0.

H. Copyright 1988 animals in seminatural environments. The numbers of subjects were too small (4 per group per adult hormone o treatment) for comparisons between groups to reach F-OIL-TP F-TP-TP M-CA-EB M-CA+TP-EB statistical significance.-W. Eliasson.) .). respectively) and from males (M) jected with EB plus P all preferred males. All females were ovariectomized and receiving ences (de Jonge et al. L. 1988). and the other half with EB plus P. *p < . significant.. Neither of the castrated (CA) at 24-36 h after birth and given oi! or TP on Days 2 groups gonadectomized on Day 60 showed any prefer- and 4 (Groups M-CA-EB and M-CA+TP-EB. tion of the groups. Johnson and Tiefer (1972) i= r. another third was ovariec- tomized at 30 days and given an E implant between 30 q) and 90 days of age. 451-460). Used by permission. Kaye and M. the two remaining groups were not different from each other. females are proba. com- pared with nonandrogenized intact or sham control females. Day 60 ovariectomized females in- injected with oil or testosterone propionate (TP) on Day 5 (Groups F-OIL-TP and F-TP-TP. Muntjewerff. 1983). data shown are from tests con. All females were treated i= 20 Ö with TP from 104 to 125 days and then tested. & Caran- 50 o Stimulus Male • Stimulus Female zaro. Altematively. Allofthe . Males seek out burrows of females and are permitted in the burrow if the female is proestrous. J. used a modified T-maze apparatus with astimulus female " Cl . males castrated I- ~ 0 on Day 1 or Day 60. Copyright 1980 by Pergamon Press. and N. 22. q) The groups tested induded intact males. respectively). and females ovariectomized on Day 60. In - addition. but were different from all the other groups. All preferences in eitber direction were statistically if injected with EB plus P. pubertal E treatment appeared to have induced Intact E tmptant $ham Intact E Im plant Sham Control Controt a preference for females. Ciaccio.Vi 25 in heat in one goal box and an intact male in the other . and such Figure 2. J. pp. Little is lrnown about the social organization of wild de Jonge. M. 1987). by Academic Press. Thus. In A.. 1988. testosterone propionate at the time of testing. Females ences when injected with heterologous hormones (EB plus were ovariectomized before testing.) o Stimulus Male • Stimulus Female 40 * * * * that of control females. the Non-Androgenized Androgenized effect might be experiential (de Jonge et al. most Figure 1. (Data from "Sexnal behavior and sexnal orientation of the female rat alter hor- monal treatment during various stages of development" by F. E. 25). Development 0/ Responsiveness to Steroid Hormones: Advances in the Biosciences (Vol. The Day 1 castrated males ducted following TP (female Groups F-OIL-TP and F-TP-TP) or preferred females if injected with TP but preferred males estradiol benzoate (EB) treatment (male Groups M-CA-EB and M- CA+TP-EB).05. Data shown are from females (F) preferred females. Of the control groups. and J. half of each of the other groups was injected with TP. but nonetheless the results were dear enough to be interesting. 1980.338 ADKINS-REGAN RATS bly solitary and are quite aggressive toward males except during proestrus and early estrus (Lisk. P for males. The pair is together for about a day before the female evicts r- r. To determine if early castration changes the sexual q) E preferences ofmale hamsters. the intact males were injected with oil. for Females Females the females had been given tests for mounting immedi- ately prior to the tests for sexual orientation. neo- natal androgen induced orientation to female stimuli. E = estradiol.j? r- groups except those receiving neither early androgen nor pubertal E significantly preferred females (Figure 2). Louwerse. Meyerson. This may represent a very in- teresting kind of "late" organization. TP for females). Percentage of test time spent with stimulus males versus females by female subject rats. Percentage of test time spent near stimulus males of the intact and Day 60 castrated males injected with TP versus females by subject rats. Hetta (pp. the male from the burrow. using HAMSTERS (Mesocricetus auratus) female percentage minus male percentage as the measure. and the final third was ovariectomized E r- at 30 days and sham implanted. M. See text for a descrip- experience is known to modify female rat sexual prefer. Kaye (Eds. Used by pennission. Prior to testing. (Data front "Sex-Specific Orientation in Female and Male Three points can be conduded from these results: ham- Rats: Development and Effects of Early Endocrine Manipulation" sters receiving homologous hormone replacement show by B. A. but based on observations of laboratory-reared Poil. Hormones & Behavior. One-third of each group was r- ovariectomized at 90 days. van de hamsters. 100-115.

tomized female brought into estrus with an E implant. Females implanted with the high T dose males. gonadeetomized at 5 days and given high. 1985). follow- Q) ing adult TP. they showed no preference. do. None ofthe groups ment spent more time near both kinds of males than near showed any significant preferences for one sex or the other females. 167-176. (Data from "Neonatal exposure of planted females. Stockman. females gonadeetomized at 5 days. ANIMAL SEXUAL ORIENT ATION 339 distinct opposite-sex preferences. Q) 10 f- monal factors also shape later sexual preference. preferred castrated males to females. Tbe ing. rather than E showing no preference as females given adult TP would i= u. procedural replacement showed no preferences. E (some females). early cas- tration did not completely sex reverse the males. they still preferred females. Percentage of test time spent by female ferrets near implanted females from the day of birth to Day 15 with stimulus males versus females. heterologous hor- mones do not reveal these preferences. T. males. All subjects were gonadeetomized at female ferrets to testosterone alters sociosexual preferences in adult- 11 weeks and tested without hormone replacement. and control females reeeiving adult E or E plus following adult T. early castrated predicted. which two stimuli: a sexually active intact male and an ovariec. ~ 0 FERRETS (Mustela furo) Two experiments (Martin & Baum. With homologous hormone ence for males is sexually differentiated (Figure 4).) gonadeetomized at 11 weeks and treated with T (males). and thus fell in be. males given adult T preferred females. (1985) used a T-maze apparatus with treated females did not choose like control males). T and again following injeetion ofEB. Ad.or low-dosage plants. in that. castrated on Day 5 chose males more often than males males. and an intact male implanted T implants either from 5 to 20 days or from 20 to 35 days. Tbus. an androgenic or estradiol (E) on tbe day of birtb. and early T- Stockman et al. but DHT had no ef. ovariectomized at 11 weeks wbo were not receiving bormone re- planted with cholesterol or with empty capsules and unim. The manipulations never com- females given adult T would prefer females. indicating that T during development masculinized preferred intact males and females about equally. D Sllmulus Male ~ lntacl • Sllmulus Female and early castration of males results in female-like prefer. Males replacement females prefer males and males prefer fe. Martin and M. like ences of males. & Baum. The tbree noncontrol groups were impIanted witb testosterone (1'). Controls included females im. bood" by J. T. What cannot result in part from the influences of sex hormones between be told from this experiment is whether early T -treated 5 and 20 days after birth. Callaghan. or E. implying that hormones prior to Day 1 or nonhor. 11. (In Martin & Baum's. Martin and Baum (1986) Figure 3. but males show no preference. or E plus P (other females) before test. 5-alpha-dihydrotestosterone (DHT. Control males without adult hormone ment. adult T [Stockman et al. males castrated at 5 or each stimulus was recorded. 1986. Tests were conducted in a square arena with four following groups were tested: control males and females stimulus animal compartments. experi- P were no different.) Following adult EB. Early treatment with indicating that early castration feminizes the sexual prefer- T masculinized the preferences of females. which means that adult hormone exposure influences sexual preferences. could mean that prenatal as weIl as postnatal hormones . placement at tbe time of testing. indicating that testicular hormones seereted between 20 Day 1 and Day 60 are an important determinant of the normal male preference for females.. 5-alpba-dlhydrotestosterone (OUT). control fe- changed this lack of preference to a preference for an es. males did not choose like control females. and the time spent near gonadeetomized at 35 days. T. with T. ditional control unimplanted males and females were Used by permission. • Stlmu rus MaJ8-CaSlrated ences foUowing adult treatment with female sex hormones. a castrated male. 1986. 1985) have established the European T DHT E ferret as a valuable species for studying hormonal in- fluences on sexual preferences. Baum. Results sbown are from females metabolite of T). as would be pletely reversed sexual preference (Le. These results show that sexual preferences of ferrets tween early T-treated females and controls. Copyright 1986 Pergamon Press. whereas without replacement females still prefer castrated at 20 days or control males castrated at 35 days. 1986. making hamsters a good FEMALE FERRETS species for studying sexual preferences.. Early E-treated females males. Animals were tested as adults following implantation with Control females not reeeiving adult hormone replace. Psycho- neuroendocrinology. but sexual preference. males preferred males and chose males more often than trous female stimulus. from 5 to 20 days chose males less often than control fe- feet on preferences (Figure 3). but spent the same differences are believed to account for this discrepancy amount of time near all the stimulus animals. Stimulus animals were two 20 days. indicating that this prefer- preferences in this situation. control ferrets show sexual did any of the male groups. and females ovariectomized females brought into estrus with E im. However.

A. (Frädrich. 20 (M-20).340 ADKINS-REGAN FERRETS ovariectomized as adults and were tested during two periods: first with a stimulus male after receiving EB. S. pp. (tests with stimulus males) or testosterone propionate (tests with or during both periods. 100 . and Dunbar (1977) tested fe.05 compared with same-sex controIs (Group M-35 or FEMALEDOGS o • F-3S). pp. 1985). Dunbar. Wolves. 1985. 409-414. the wild ancestors of dogs. Although free-ranging urban male dogs all attempt to mate with an estrous female. 711-715. 1974. conc1usions to be drawn about sexual orientation.. Callaghan. However. 1977. R.) . Results shown are for tests following adult injection of estradiol benzo- ate. in infancy.:: 75 times. form long-term monogamous pair bonds (Klei- man. Both wild and domestic dogs are rela. 1977). Males are allowed males were chosen by ferrets. dog. inc1uding untreated controls. F.and postnatal T might be impor- ~ 0 tant for the differentiation of sexual preference in dogs. Gründlach. (Data from "Effects of Neonatal Castration and Testoster. because adult sex hormone treatment varied with stimulus sex and ~ the two stimulus sexes were presented at rather different . Physwlogy & Behavwr. Copyright 1985 Pergamon Press. or 35 (M-3S) days and females (F) ovariec- tomized at 5 (F-S) or 35 (F-3S) days. Used by permission. were American Psychological Association. Er- 300 • skine. (Data from "Hormonal Control of Sexual Attrac- tion in Pseudobermaphroditic Female Dogs" by F. the '0 results suggest that pre. Stimulus Male one Propionate Treatment on Sexual Partner Preference in the Fer- Slimulus Female ret" by E.) - contribute to sexual preference in this species (Baum. Percentage of trials in which stimulus males versus fe. Stockman. Estrous female beagles strongly prefer to mate CONTROLS T·I T-U with some males rather than with others (Beach & Figure 5. Johnson. Copyright 1977 recorded. *p <. Baum. in utero (U). Anisko. Time spent in a 6OO-sec test visiting a tethered stimulus LeBoeuf. Subjects were males (M) castrated near the group only during the breeding season. J. This rever- sal was greatest with combined pre. Group F-5-T received a rela- tively high dose of testosterone from Days 5-20. Anisko. Journal 0/ Com- and the total time spent "visiting" the stimulus was parative & PhysiologicaJ Psychology. 34. Stockman. this is not a design that allows direct (/) . and I. 1983). J. and that further research on this species is highly • desirable . suggest- 100 ~ Stimulus Female ing areversal of sexual orientation (Figure 5).and postnatal T treatment. implying mate choice on the part ofthe o '--- female. DOGS (Canis familiaris) (/) "0 C o ~ 200 • Domestication seems to have had a marked effect on (f) the mating system of dogs. only some males are successful (Daniels. 1968). Used by permission. 50 n • M·5 M·20 M·35 F·5 n F·5·T F·35 PIGS (Sus serofa) The basic unit of social organization of wild pigs in Eu- rope is a small group of females with their young Figure 4. in infancy (1). domestic dogs appear to mate somewhat promiscuously. or during both periods (U+I). 91. but all three early androgenized groups spent more time with females than with males. R. Beach. 1967). male was tethered in the center of a circular outdoor arena. tion suggests that mating is far from indiscriminate. All females. then o Stimulus Male again with a stimulus estrous female after receiving TP. J. Controls spent more time with males (after EB) than with females (after TP). . 400 . A stimulus male or estrous fe. In contrast. As adults Beach. although systematic observa. producing possible order effects. A. The three noncontrol grouJlS were treated with T (testosterone) tively monomorphic. I. Strictly speaking. and M. subjects were ovariectomized and given either estradiol benzoate males that had been treated with T in utero. Johnson. Estrous at 5 (M-S). stimulus females). & Lundell.

males were castrated with EB from 3 to 5. Ford. and males castrated at 2 weeks and implanted In an experiment by Ford (1983a). they spent mucb Tbe results of these experiments in pigs suggest the fol- time near the stimulus male. Wild and domestic pigs ofboth sexes 500 engage in courtship or proceptive behavior before copulat. as velopment.) of sex hormone influences earlier in development. 1987). at age 4 months. males show no consistent preference CI) "0 300 c: and spend relatively little time with either stimulus. but not males.5 months. The results are shown in Figure 7. Anatomical sexual differentiation is complete weH as androgens (Ford. because while standing near the male the fe- male adopts the receptive posture seen during I F-8 M-48 M-4 M-8 copulation-immobilization with the ears cocked. J. show subjects were gonadectomized 48 h or less after birth (M-48) or at a distinct highly estrogen-dependent sexual preference in age 4 (M-4) or 8 (F-8 and M-8) months. As hypothesized. control males castrated at 5. such as estradiol. feminized and. * r- ing (Signoret. 1983a. Males castrated at 4 or lowing conclusions for this species: sexual orientation is 8 months spent less time with the male and more time with sexually differentiated. tested biweekiy in a modified T -maze with intact male males castrated late were uninterested in stimulus males. Figure 6 shows the results from the second EB implants masculinized the sexual orientation of both trial. males castrated at son. 6. ing development are an important determinant of these Based on the results of this experiment. Males castrated as adults and given an EB injection do not show Figure 6. testicular hormones produced dur- the female. Beginning at age within 48 h ofbirth. However. 152-162. Does estradiol before birth (Elsaesser. hormonal organization of sexual early-castrated males treated with sex steroids postnatally preference is possible surprisingly late in development. Ford. Wild pigs are much more dimorphie physieally r- than rodents or dogs. tween males and females in these choiee tests is a result pp. females. it is important to know that ual orientation has not yet been studied in pigs. pigs were injected with EB and As expected on the basis of Ford's (1983a) experiment. 17. Male (M) and female (F) tests. Copyright 1983 Academic Press. with estradiol benzoate before testing. all subjects were injected choiee tests. as is typical of highly defeminize sexual orientation during juvenile development precocial animals. females or sexual preferences. 100 * I spending most of the test standing near hirn. 0 StImulus Male • Tbe sexual preferences of pigs have been systematica1ly 400 investigated by Signoret (1970). females ovariectomized at 3 to 6 months to males castrated shortly after birth 2 months and implanted with EB from 3 to 5. 1988) (permanent?) feminization of copulatory behavior (Berry in which the following groups were tested: control females & Signoret. pair bonds are unlikely. each subject was injected with EB and given trols). should be masculinized and sbould not prefer males. Orgeur.05 compared with M-4 or M-8. like the control females.5 months. 1982). sexual orientation. Males castrated shortly after birth were quite females and early-castrated males. the insufficient. Hormones & Behavior. Thus in this species. or at 8 months (con. & Signoret.5 months. Nor o u r- do males markedly prefer estrous to nonestrous females. rather than a general social preference. 1982). produces long-Iasting defeminization (Ford & Christen. and PIGS males mate with more than one female. This seems to be a sexual preference. (Data from "Postnatal Differentiation of Sexual Prefer- Two experiments have shown that this difference be. ANIMAL SEXUAL ORIENTATION 341 females probably mate with more than one male. Time spent by pigs in the stimulus male versus female this behavior and do not spend time with males in choiee end of a T -maze during two S-min tests.5 months. 1970). . the pig seems to be an exception to the usual rule that male pigs. *p < . produce very large amounts organizational hormone effects occur only early in de. In choice tests conducted SlImUlus Female in large modified T-mazes with intact male versus nones- trous female stimuli. Tbe dose of EB was and males castrated at 2 weeks resembled control females then increased for a second trial because it seemed to be by orienting to the male stimulus. Used by permission. Tbe and estradiol rnay be involved in the differentiation of male effect of androgen treatment during development on sex. yet castration of males as late as 4 in this species? This question has been addressed in an months after birth (early puberty) can produce long-lasting experiment (Adkins-Regan. 1984. Beginning at 12 months. Female controls were ovariectomized at 8 months. To un- derstand these experiments. T treatment given from ovariectomized at 2 months. versus ovariectomized female stimuli. (more than 40 pg/rnl) of estrogens. even juveniles. T -maze choice tests. 1983b). However. CI> Cf) 200 Nonestrous females behave quite similarly. ence in Male Pigs" by J. es- trous females or ovariectomized females given a single EB injection show a marked preference for the male. 2 weeks. they sbowed no preference.

1988 & Conaway. Birds that are paired Chevalier-Skolnikoff (1976) described sexual interac- clearly indicate their status to human observers by several tions between males and between females in heterosex- behaviors. cal contact with each other. and tested for sexual and other social behavior. Akers & Conaway. P. 1987). 1976) a11 other groups were gonadectomized at 2 months (females) or 2 weeks (males). most finches pair with an opposite.) Q. . Fe- males remain in their natal troop. 1986). it would be interesting to see if females' mous pair bonds. although extrapair copulations are oc. 200 Some of these early EB-treated females actually succeeded in pairing with other females. take an active role in mate selection. Sometimes 1967). stead. the behavior occurred mainly between animals with jected with EB during the first 2 weeks after hatching.5 months (and thus intact during development). M-EH and F-EH were implanted with estradiol ben. 1970). build. similar. yet Q) cn preferred males). Although the mounter was usually (manuscript submitted for publication). Chevalier-Skolnikoff. the behavior itself seemed much more sexual than agonistic. preferences for other females over males as partners de- casionally seen in the laboratory. 8 of the females mounted other females extensively (Akers tive Behavior in Pigs: Defeminizing Effects of Pubertal Estrndiol" by E. M-IN are species of wild and captive primates (for references. Although the early EB treatment itself clearly changed the sexual orientation of EB-treated females (the (/) "0 c 100 0 U control females were also raised in unisex cages. see males castrated at 5. varied as a function of menstrual cyde stage. whereas males disperse before adulthood. In a recent experiment (Adkins-Regan & sometimes be predicted by knowing dominance status. Signoret. All the subjects in this experiment were reared in uni- sex cages. like heterosexual mounting. and being in a nest box together (But. and J. *p < . and female-female sexual interac- TP. but it masculinized the preferences ofthe females. The birds nest colonially. 1986. male and female zebra finches were in. 10- Ascenzi. Homosexual mounting. implanted with in rhesus macaques. the birds were gonadectomized. 1979. Adkins-Regan. (Data from "Sexual Differentiation ofReproduc. Dominance interactions M-EB M-CA F-EB F-OV M-IN among the males play an important role in determining who gets to mate with a given female.5 months. females were The behavior and soeial organization of zebra finches mounted most frequently during the periovulatory period are very similar in both field and laboratory (Immelmann. implying minimal if any testing procedure included introdueing each subject into hormonal control. and form long-term monoga. CO ~ The various species of macaques live in groups con- sisting of females and their young together with several adult males (Melnick & Pearl. preening each other. the more dominant of the 2 females. 7 out of (M-CA or F-OV). As in the rhesus macaque observations described terfield. 1979).. females usually mate with males who -10e have emigrated into the troop. MACAQUE MONKEYS (Macaca spp.05 compared with same-sex controls (Macaca mulatta) housed in an outdoor corral. and observing the subject daily. Time spent by pigs near the male barrier minus time Homosexual interactions have been observed in many spent near the female barrier during 5-min choice tests. ual partners. Heterosexual mating in this spe- Controls were injected with the vehicle. 1985). ual groups of stumptailed macaques (Macaca arctoides). its duration and pronounced genital focus dearly distinguished it from the brief mounts that serve a dominance function in this Spe- ZEBRA FINCHES (Poephila guttata) cies. above. Copulation itself is relatively infrequent. such as spending a great deal of time in physi. and least frequently during the luteal phase. All subjects were injected with caques. it is possible that it has this effect only Q) CO " if the finches also experience unisex rearing. The tions were similarly independent. Figure 7. In a heterosexual group of rhesus macaques EH prior to testing.342 ADKINS-REGAN a colony cage containing breeding pairs and unpaired birds PIGS of both sexes. mainly by preventing the target females from being able to pair with males. Richard. the behavior did not occur in aggressive contexts. Male-male and female-female interactions were very ing a nest together. The early EB treatment had no effect on the pairing choices of the males. although who mounted versus who was mounted could sex partner. strong affectional ties. After reaching eies is much more independent of female cyde stage than puberty. E I Q) u. are sexually dimorphic the females appeared to prefer females to males as sex- in plumage and beak: color.Orgeur. and have been described in detail in two species of ma- wate (EH) from 3 to 5. In the laboratory. Both sexes appear to pends on cycle stages. but occasionally with ex- tratroop males (Smuts. P.

conclusive either because there were no controls or ble of initiating and participating in sexual interactions because the subjects were too young to have a well- with either sex. the early androgenized females when possible. however. the subjects' own sisters. Of 10 comparisons. & Goy. relevant information comes from an experiment (Pomer. indicating that these behaviors are in fact old women. and all groups were given an estradiol progesterone. and in control females. 30-year- trol females. Information relevant to sexual orien- orientation. interviewed a group of women over 17 years of age who normally low androgen produces men that prefer other had congenital virilizing adrenal hyperplasia (CVAH). erotic imagery. The authors present several arguments in favor distinguish between a change in sexual orientation and a of a hormonal explanation for the results. Green. whereas the other 5 were exclusively heterosex- posure to excess androgens during fetal life produces ual. engag. gens prenatally but not postnatally. were not included in the study. two obtained posi- ual orientation had been noticed. abnormal hormone levels in adulthood as well as pre- ing in homosexual interactions does not necessarily im. The most sies. as was the case for these subjects. who are excel- scored lower than control females. 1980). 1982). They also point out that because DES women sometimes have abnormal Obviously. neither involving excess androgen. Others found no differ- sistent preferences for homosexual over heterosexual ence between exposed and control subjects. or DES plus gonadally intact. ically masculinizing progestins before birth (Money & mones during early development might change sexual Matthews. as is desirable in this kind ofresearch. 1985) in which proceptive had been treated with the synthetic estrogen diethylstil- behavior toward a tethered adult male was measured in bestrol (DES) during pregnancy. and it has been hypothesized that ex. 6 were significant when the controls were unrelated tation in female rhesus monkeys. and Lewis (1984) women that prefer other women as partners. the data do not distinguish between act1y comparable to these animal experiments. anatomically masculinized rhesus females born to mothers and Williams (1980) found no difference in the incidence treated with TP or DHTP. but com. of these four recent studies. (1985) interviewed DES-exposed 17. were more likely to have had homosexual imagery and Ehrhardt and Meyer-Bahlburg (1981) reviewed many experience. homosexuality) for most comparisons. drogen and insufficient corticosteroids. natally. tation was available for only 6: 1 had had no erotic ex- tally in humans. Controls were non-DES-exposed women sexually differentiated in this species. Thus. Kester. 1981. normal levels of sex hormones to see if any effect on sex. the males had lower scores than the con. These results suggest a pos. one is a foIlow-up of cal treatments with controls matched on other dimensions 12 women aged 16-27 who had been exposed to anatom- can reveal whether excesses or deficiencies of sex hor. and for the third measure (solicits per minute) they former had higher scores (indicating more bisexuality or were completely deferninized. sible effect of early androgen exposure on sexual orien. Finally. such in- many mammals (Feder. they might ation. Goy & McEwen. The females were left exposed prenatally to DES. paring people with certain endocrine disorders or medi. however. CV AH women feminize males and have little effect on females. For three of the four from the same clinic who had abnormal Pap smears or. dividuals are exposed to abnormally high levels of andro- then they should masculinize women and have little ef. Schwartz. and overt sexual behavior. Two of these studies examined people whose mothers antz. and that ab. tive results in support of a prenatal hormone hypothesis . for two of these their lent controls for this kind of research. an adult and a prenatal hormone hypothesis. The effect of prenatal exposure to genetic disorder in which the adrenals produce excess an- excess estrogen in rnen or wornen is harder to predict. even when both are possible. et al. Unfortunately. perience. 1988). implant prior to testing. When compared with fect in men. but additional research women. if they do not or if they interfere women with two different disorders of sexual differenti- with the actions of endogenous androgens. in males castrated shortly af. Four studies done since Ehrhardt and Meyer-Bahlburg's Can early hormone exposure lead to such preferences? (1981) review have direct1y addressed the prenatal hor- There are no experiments in which hormones have been mone hypothesis. Anatomical differentiation takes place prena. activity. Of the two other recent studies. and thus are quite confounded in terms of testing ply a homosexual orientation. endocrinologically normal macaques are capa. medically normal controls of the classic studies of people prenatally exposed to ab. we cannot expect to find human studies ex. The males. only 1 of the 30 DES women had been nearly exclusively HUMANS (Homo sapiens) homosexual throughout her sexualiife. adult hormone levels. Money. Kinsey rating scales scores fell between control females and early castrated were used to compare the DES and control women. Some examined people exposed to not highly sexually differentiated. Thornton. Ehrhardt tive behavior. Iftreated shortly If estrogens mimic androgens in humans as they do in after birth. ANIMAL SEXUAL ORlENTATION 343 Thus. Roy. Finch. that this hormonal influence is relatively minor. a prenatal hormone hypothesis. All four assessed sexual orientation by manipulated early in development and sexual preferences gathering information in interviews about sexual fanta- have been assessed in choice tests in adulthood. of homosexual behavior between control men and men ter birth. as if sexual preferences and behavior are developed erotic life. and 2 were significant when the controls were with both male and female stimuli would be necessary to sisters. Furthermore. which would require con. For all four measures ofprocep. The controls were not as weIl matched. proceptivity measures. a men (Dörner. Some studies were in. but point out reduction in sexual motivation.

both sexes of hormone exposure causes demasculinization of copu- dent on adult activational hormones. in that they prefer to spend zation of copulation fit sexual orientation as weIl. *The preferences of males were not measured. Masculinization refers to decreased preference for males and/or increased preference for females. monogamous mating systems or pair bonds (although tion is particularly interesting in this context. Descrip- time or pair with the opposite sex. 1985 Dog Not yet known Complete masculinization (T)?* Beach et al. and did so without hormone manipulations on the sexual preferences of masculinizing the copulatory behavior of the females animals. but do not tell us whether this labil-lasting or permanent. E = estradiol.or early postnatal rather than demasculinizing it in males. 1987). Genetic wolves. and pigs. in. in that they are lation (it makes males female-like by decreasing male- reduced by gonadectomy or are different in gonadec. or are they merely two reflections of the same underlying process? These experiments have established that in laboratory One way to approach this question is to exarnine tests. Peter- son. but one of these two did not include of mammals and birds. are produced by steroid hormone ity is possible because the individuals who changed had actions relatively early in development. 1983a Zebra [mch Not yet known Masculinization (E) Adkins-Regan & Ascenzi.deferninization (Adkins-Regan. In zebra finches. and result in be- been exposed prenatally to testosterone (lmperato. 1980 Hamster Feminization Not yet known Johnson & Tiefer. ical masculinization occurs (lmperato-McGinley.. and finches exhibit whether descriptions of species differences in the organi- clear heterosexual orientation. ferninized and early T -treated females are masculinized. sent from Table 1 are any studies of mammals with One naturally occurring disorder of sexual differentia. 1981 Meyerson et al. sex hormones produced during any normal controls. Analogous experi- ical abnormalities (and who know they do) may not be ments with macaques and humans are suggestive of a sirni- relevant to the problem of explaining sexual orientation lar effect but are not yet conclusive. Table 1 also reveals that the total number of ex- low levels of DHT and are quite female-like in anatorni. of males or early T treatment of females or both have been Another way to compare early hormone effects on sex- found to partially or completely sex reverse sexual orien. whereas males show no reliable prefer. and have later married women (Herdt & Davidson. at which point marked phys. E treatment masculinized sexual preference in females. But how far does this parallel extend? Are there any im- son. In each of these species. orientation.typical copulation) rather than masculinization or tomized animals receiving homologous and those receiv.tween the differentiation of copulation and sexual ences for either sex. chickens..344 ADKINS-REGAN of sexual orientation. to the weIl-known organizing effects of early sex steroids 1988). tors such as higher societal status for men (Herdt & David.5 months (early puberty).tions that include birds do reveal a major discrepancy be- rets prefer males. deterrninant of adult sexual orientation. . in anirnals is surprisingly small. and zebra finches. periments on hormonal organization of sexual orientation cal appearance until puberty. tTreatment given from 3 to 5. Gautier.. are monoga- males with 5-alpha-reductase deficiency have abnormally mous). 1979). havioral sex reversal such that early castrated males are McGinley et al. These observations suggest considerable lability on copulatory behavior per se. In rats. Many ofthese individuals Comparisons with the Organization of that have grown up as girls subsequently live as men. hamsters. 1987 Note-T = testosterone. In quail. Feminization refers to decreased preference for females and/or increased prefer- ence for males. 1987). 1979) or because of sociocultural fac. observations ofpeople who have med. hamsters.. in that the effects are long in sexual orientation. ing heterologous hormones. Copulatory Behavior cluding some that have been married at a young age to Most of the results summarized in Table 1 are sirnilar men. 1977 Pig Complete feminization Complete masculinization (EH Ford. see also discussion in text of the experimental design. Furthermore. early these sexual preferences have been shown to be depen.ual orientation with its effects on copulatory behavior is tation. 1988). Conspicuouslyab- in people without such abnormalities. as Ehrhardt et al. the wild ancestors of domestic dogs. Female pigs and fer. Table 1 summarizes the effect of pre. It is possible to conclude that in several species to consider the timing of the critical periods for sex rever- Table 1 Summary: Hormones and Sexual Orientation Effect of Early Effect of Neonatal T or E Species Castration on Males Treatment on Females References Rat Complete feminization Masculinization (T) de Jonge et al. portant differences between sexual orientation and copu- lation with respect to the role of hormones in differentia- DISCUSSION tion. either early castration (Adkins-Regan & Ascenzi.. & Sturla. 1986 Stockman et al. ferrets. 1988 Eliasson & Meyerson. 1972 Ferret Partial feminization Partial masculinization (T) Martin & Baum. neonatal or juvenile (pigs) development are an important (1985) cautioned.

. however. step for understanding the biology of sexual orientation noret. sons why it is difficult to apply animal models to the hu- In several mammals. failed to masculinize the sexual preferences of fe. periments on effects of early hormones. however. Does adult sex hormone levels of homosexuals are normal for sexual orientation share the same pattern of steroid speci. For example. David. Our failure to understand the ori- dimorphism. have instead focused on deeisions about with which spe- tation can be reversed without altering the genitalia) and eies to mate or with which individual from among oppo- zebra finches (who have no external genitalia) are either site sex conspeeifics to mate (Bateson. Gooren. The fact that both sexes show significant sex. defeminization of receptivity was not. because while DHT. Meaney. Pigs tion of its usefulness with respect to understanding hu- have the advantages of obvious physical dimorphism and mans. rats and hamsters) is a problem. 1978). pigs (in which sexual orien. In the Meyerson et al. 1980). the best answer is no. orientation. reversal of sex- et al. 1988. E was only partially effective. However. The dearest example of a difference between the two mals. 1988). gued that animal experiments in which the early treated ment are equivocal with respect to an aromatization animals are left intact. Meyer-Bahlburg. but primates. sexual behavior can occur outside of the periovula- critical periods can be seen in the pig. minants of sexual orientation might weH be different in mates have the potential to be particularly good models different species in ways that can be predicted from the for human sexual behavior. 1984). they are an important first that are activated by E alone rather than E plus P (Sig. It is unfortunate. 1970). The developmental deter- son. ual preferences. Males castrated tory period. the critical period Meyer-Bahlburg (1984) provided two additional rea- ends at different times for these two behaviors. because of the ing development. but in opposite directions. Whether sexual orienta. seen. Pri. very few studies of sexual orientation in any nonhuman ticular hormones was already complete at 4 months. therefore. (1980) ex- Thus experiments on finches and pigs make it dear that periment. suggesting that sexual behavior has social/ at 4 months were receptive when mounted by stimulus affectional functions other than reproduction in the strict males but did not prefer males in the choice tests (Ford. The sexual orientation to actively choose a mate. 1984). there relatedness and because. the experiments masculinized sexual preference in pigs (Adkins-Regan reviewed here show that even in animals. The fact that The Psychobiology of Sexual Orientation little is known about the mating system of wild ferrets The value of research is not. 1983). Goy & McEwen. Regardless of whether these animal experiments easily measured very dear female preferences for males shed any light on our species. in contrast to most other mam. and possible in- man phenomenon. without any alteration in sexual anatomy (Ford. that there have been I 983a) . AN IM AL SEXUAL ORIENT AnON 345 sal. E strongly for human homosexuality. whereas human Each of the species that has been used has advantages homosexuals are anatomically normal. may be more developmental constraints on sexual prefer- . makes rats. 1984. In pigs. defeminizes copulatory behavior via conversion to estro. hamsters. and zebra finches good choices. which cannot be aroma. Moore. both because of phylogenetic mating system and social organization. sexual orientation in nonprimates and teractions between that environment and hormones (see humans is simply not homologous (Beach. but the effect of T on the sexual orientation ual orientation does not necessarily require heterologous of this speeies has not yet been determined. are actually preferable if the goal is models male ferrets. Also important ing human sexual orientation? It may weH be that for all will be studies of the role of the social environment dur- of the nonprimates. 1979. foolish or wise choices. 1979. Thus masculinization of sexual preference by tes. culinized when tested foHowing either EB or TP in adult- ual orientation independently of copulation: these are hood. Viewed in this way. their biological sex. many animal behaviorists interested in mate choice. and in the Adkins-Regan and Ascenzi (1987) separate categories of behavior. 1981. Zebra finches offer distinctive plurnage in the animal kingdom. neonatally EB-treated female finches tion can also be dissociated from courtship or proceptive preferred female partners regardless of whether they behavior by early hormone manipulations remains to be received EB or TP as adults. although quite confounded if the hypothesis. the individuals are anatomically as Animal Models of Sexual Orientation weH as behaviorally sex reversed. for that matter. sense. 1983a). early T masculinizes or man situation. cies mating preferences (Bateson. who ital component of sexuality. pronounced pair bond behavior. First. purpose is testing any organizational theory of sexual tized. neonatally androgenized female rats were mas- sex hormones acting during development can change sex. and a gins of sexual preferences in humans is matched by our monogamous mating system in which both sexes appear ignorance of them in animals. and disadvantages as a model for sexual orientation complete reversal of sexual orientation has been obtained research. experiment. Such understanding will require more than simply ex- Are any of these species suitable models for understand. a simple func- (or. hormones in adulthood. which is known to be important for spe- profound cognitive and emotional components of the hu. and E itself mimics the ing to receive heterologous hormones in adulthood. the effect ofT (Feder. it could be ar- ficity? The results of Martin and Baum's (1986) experi. Meyer-Bahlburg's (1984) second point was that in the animal experiments. both ofwhich deserve reevaluation. humans can have homosexual preferences without hav- genic metabolites (aromatization). Depending on whether the dimension of mate choice has been neglected even by the researcher wishes to emphasize or deemphasize the gen.

(1983). and possible social functions. 967-972. Science. (1967). Journal 0/ Comparative male ferret. ELUS. Hormones and brain differentiation.. Con- male dogs.). & VAN of male and female zebra finches treated with oestradiol during the OE POLL. J.I. I. R. A. OVERDIJK. 88-119).. Newman. J. authors witnessed 555 instances of heterosexual court. Sexual orientation after prenatal exposure to exogenous es- 230. P. The pair bond in the zebra finch. FEDER. & DUNBAR. F.. In D. Endocrine control of behavioural sexual differentiation in the approach behavior in male laboratory rats. Foxcroft (Eds. ORGEUR.). W. 93-116). P. . S. 59.. Sexual behavior and sexual orientation of nestling period. H. H. Elsevier. Science. E. 37. 91. S. as has been shown for female- OE JONGE.). J. New York: Plenum Press. Archives 0/ Sexual Behavior. H. 517-522. M. Biological determinants of sex: their scope ing. cal Bulletin. F. 3. Differentiation of coital behavior in mammals: prenatal sex hormones on gender-related behavior. M. (1984).346 ADKINS-REGAN ences in monogamous species. M. A comparative analysis. Neurohormonai functioning and sexual BEACH. Sexual experience and preference for males 1987). (1987). & HUNT. 285-289. C. ANISKO. A. In J. G. Chichester. Diversity and evolution of behavioral controlling mechanisms. sion of sexuality in wild animals studied in the field CONOVER. 8. L. AKERS. S. orientation should inc1ude greater attention to this dimen. F. S. H. 1982). M. 1. 1312-1318.. 10. P. new series. Biology 0/ Reproduction.. (Ed. (1981). E. Early experience and sexual preferences. Famer. Applied Animal Ethol- which resulted in c10acal contact. P. N. In N. Nutrition et Developpement. FORD. Social belwviour in birds and mammals (pp. (1981). LHRH and mating behavior: (pp. (1985). ogy. female pig and sexual differentiation of the stirnulatory oestrogen feed- Hormonal control of sexual attraction in pseudoherrnaphroditic fe. DAVIDSON. 369-383. J. differentiation in heterosexuals. Areport by Jarnieson and Craig (1987) Condor. Pharmacology Biochemistry & Behavior.. some of dogs: 11. STOCKMAN. J. (pp. M. the Prentice-Hall. LoUWERSE. L. Homosexual behavior in a labora- Finally. ZIMMERMAN. Cambridge. (1987). (1985). S.. Trends in tion. Cambridge University Press. Animal Belwviour.. VERIDIANO.).546-558. E. P. 17. Sex play and behavioural sexu. Marine animals that congregate in groups rats to sex odors. & ASCENZI.. 511-527. During CREWS. 472-476. An evolutionary perspective. In R. A.. and 41 homosexual interac. Neu- I. (1987). Coital behaviour in dogs: ment of sexually dimorphie behaviors. Early organizational effects of hormones: preference.. (1987). EHRHARDT.. Crews (Ed. LoEB. 57-77. H. or females in the female rat. CHEVAUER-SKOLNIKOFF. & WILSON. A. ROSEN. J.. receptivity and proceptivity. 57-75. L. Psychobiology o/reproductive be- 3 years of observations of communally breeding pukekos Iwvior: An evolutionary perspective (pp. trogen. Journal o/Comparative & Physiological Psychology. M. J. birds native to New Zealand). 1100-1112. Androgens are specifically implicated in female rat sexual motiva- AOKlNS-REGAN. A. B. for which a "mistake" BUTTERFIELD. 24. H. The influence of estrogen. FELD- BAUM. G. 160-165. 159-228). S. 365-373.. J. H. JOHNSON. (1988). Sex. Berkeley: University of California Press. F. Hutchison (Ed. N. B. J.. L. T. In H. M. and progesterone on partner AOKlNS-REGAN. In D. Berlin: Springer-Verlag. physiological function. A. M. F. In J. KALVERDIJK.. It is tempting to hypothesize that they serve some and limitations. H. 10. pp. Experimental evidence that (Conover & Hunt. Katchadourian (Ed. BAUM. R. 249-278). A. L. ERSKlNE. F. and transsexuals.. EERLANO.. Manuscript submitted for publication. B. F. E.. 960-961. (1988). Gilles & J.. 27. 425-430. (1978). tion. (1984). Female homosexual behavior DÖRNER.. 100-115. DALY. BURGER. con- texts. Adler (Ed. 22.. Neuroscience & Biobelwvioral Reviews... 63-80. Neuroendocri. Pharmacology Biochemis- BATESON. M. A.. H. J. 370-377. A. F. F. DANIELS. In N. M. Biological determinants 0/ sexual belwviour DUOLEY. G. S. The social organization of free-ranging urban tions (12 male-male and 29 female-female). (1983). Preferential mating in the biteh. Journal 0/ Comparative & Physiological Psychol- and release gametes into the water rnight not have any ogy. R. & McEWEN. (1979). Animal models for human sexuality. E. & VAN OE POLL. (1982). Neuroendocrine response to estrogen and brain in Macaca mulatta.). 885-892.. L. (1979). Balthazart (Eds. 5. Wingfield. (1981). G. Mate choice. H. Cole & G. evolution and behavior (2nd ship/copulation interactions. D. & AMEs. The influence of methyltrienelone (RI881) on sexual orienta- Neurosciences. Human sexuality (pp. C. Psychologi- mones anti Belwviour (Ciba Foundation Symposium 62. REFERENCES OE JONGE. 142-148).. homosexuals. Hormones & Behavior. MAN. CARROLL. E. England: Wiley. M. R. ed. & SIGNORET. A. 35. 127- BERRY. E. Reproduction. alization in the pig. & LEBoEUF.). Amsterdam: 0/ pubertal estradiol. Sexual receptivity versus sexual preference. who are ex. ELSAESSER. Development of sociosexual (1985). (1985). 265-284. J. S. 507-513. ELIASSON. & CONAWAY. 211. Estrous groups and the mating system. & MEYER-BAHLBURG. (1986). J. Sexual differentiation in birds. the female rat after hormonal treatment during various stages of de- AOKlNS-REGAN. Hunt. nology 0/ reproduction: Physiology and belwvior (pp. 86. Adler (Ed. 15. A. J. 134-149). 1983). female copulations occurred during the period of egg lay. J. Endocrine control of sexual maturation in the BEACH.-P. Neuroendocrine response to estrogen and sexual orientation. M. 22. & SIGNORET.. T.. L. P. L. (1979). E. Amsterdam: Excerpta Medica. 95. Hor.). A. G.. (1965).. Neurobiology & Physiological Psychology. & TOBET. J. VAN HAAREN. F. Animal Belwviour. CARR. (1986). & MEYERSON. J. L. P. (1970). R. J. N. Physiology & Behavior. Archives 0/ Sexual Behavior. 14. New OE JONGE. Responses of Wilson. Boston: PWS. trol 0/ Pig Reproduction (pp. & Moss. 113-132). P. A. & VAN female matings in a unisexual lizard species (Crews. 47. (1983). F. orientation: A theory of homosexuaIity-heterosexuaiity. (1988).. (1977).). Most of the female. MUNTJEWERFF.. A. M. Crook (Ed. 29-54). F. London: Butterworth Scientific. N. & LUNOELL. 1984. 233-258. chives 0/ Sexual Behavior. L. Perinatal hormones and their role in the develop- BEACH. & DISSINGER. (1976).. F. (1982). York: Plenum Press.). Sexual velopment.. Effects of BAUM.). A. 158). roendocrinology 0/ reproduction: Physiology and belwvior (pp. (1976). H. MEYER-BAHLBURG. 711-715. M. & VAN OE POLL. Archives 0/ Sexual Behavior. (1979). 101.. England: try & Behavior. would be particularly costly. OE POLL.. In Sex. J. a broad psychobiological approach to sexual tory group of stumptail monkeys (Macaca arctoides): Forrns. provides a particularly fascinating illustration. -W. back mechanism. M.. E. or in females. T. (1987). A. sexual preferences at a1l. testosterone. N. (1981). 24. Testicular control of defeminization in male pigs. & female-female pairs in gulls result from shortages of breeding males. Ar- BATESON. pected to be "choosier" about selecting a mate (Daly & London: Academic Press.. Behavioral & Neural Biology. EHRHARDT. Social and sexual behaviour DE JONGE. B. E. Englewood Cliffs: (Porphyrio porphyrio. E. R. differentiation o/reproductive belwvior in pigs: De/eminizing effects DÖRNER. J. H. ERSKlNE. ADKlNS-REGAN.

England: Pergamon GooREN. G. In B. Seyfarth.. Expression of adult female patterns of sexual behavior by male. GOY. Biology of gonadal hormones. P. 0/ Biology. L. T. M. J. 9. FORD. Primate societies (pp. S. In A. endocrinology of rodents. & Behavior. W. MEYER-BAHLBURG. Syd. Animal Behaviour. (1976). (1979). (1972). Current status and future options. IMMELMANN. (1982). 54-57. '" PHOENIX. FORD. Struhsaker (Eds.. KLEIMAN. HUNT. Seyfarth. tity and psychoneuroendocrinology. W. 11. In differences in the brain: Progress in brain research (Vol. 571-576. DeVries. pp. R. rat: A methodological study of sex-specific orientation and the effects female. W. 17. & HETTA.. tation in female and male rats: Development and effects of early en- GLADUE. R. A. Biology 0/ Behaviour. B. Archives 0/ transsexuality. J. The Sambia "turnim-man": MOORE. (1988). & CRAIG. M. D. 34. New York: Freeman. Archives 0/ Sexual Behovior.. Sexual motivation in lings. 1-68. & T. In B. relation to management (Vol. L. 2.. H. V. Psychoneuroendocrinology. Corner (Eds. MA: MIT Press. tally castrated male golden hamsters. Neuroendo.. (1984).. ual partner preference in the ferret. 1. (1961). & BRAND. 105-117. W. Male-male and female-female Effects of testosterone. P. E. Behaviour. ment of the male phenotype and the evolution of a male gender iden. M. Biology 0/ Reproduction. J. 17. male groups: Genetic diversity and population structure. (1973). Switzerland: MEYERSON. L. (Suppl. 11. J. 61. B. The neuroendocrine response of luteinizing hor. K. (1987). GREEN. (1974). R.). D. 453). MARTIN. B. J. docrine manipulation. American Psychologist.. B. J. G. pp. Hormones MCCLINTOCK... ROBATAILLE. M. (1987). & LINDSTRÖM. ferrets to testosterone alters sociosexual preferences in adulthood. R. (1985). The behaviour o/ungulates and its 398). In G. Proceedings 0/ the Society tor Experimen. 11). Prenatal exposure to virilizing LoUMAN. (1984). 17. ual status and fetal hormonal masculinization and demasculinization: GRÜNDLACH. S. Amsterdam: Elsevier. (1986). Struhsaker (Eds. 33-56. masculine sexual behavior in laboratory rats. J. (1977). (1986). F. Chicago: Univer- tal Biology & Medicine. & LEWIS. Kaye & M. Neonatal exposure of female Young (Ed. Animal Behaviour. Rattus norvegicus (Berkenhout). P. D. 9-22. M. Verhaltensontogenese 46. THORNTON. L. The sexual differentiation ofsocial play. W. Acta Physiologica Scandinavica GooREN. W. Psy. J. B. 25. MONEY. CALLAGHAN. L. L. (Manuscript received March 30.). GOY. M. L.. R. DeBruin.. 1251-1253. M.. G. 269-286. E. K. Sin.) . 249-260. MEANEY. JOHNSON. S. S. B. 33.. SMUTS. (1987). Sexual differentiation o/the MONEY. OE KLERK. Acta Physiologica Scandinavica (Suppl. Baltimore: Williams & Wilkins. Roy. Brutfiirsorge. & BOUVET. Wrangharn. Estrogen positive feedback on LH secretion in progestins: An adult follow-up study of twelve women. W. (1980). A.). Develop- crine response to estrogen and sexual orientation. Science. Field observations on the ney: Angus and RoOOrtson. 347-356. sity of Chicago Press. in pigs. J.. & HARMSEN. 36. Serum estrogen concentrations during postnatal Smuts. 583-588. A comparison of OOhaviour in the Suidae. (1968). Developmental Psychobi- dohermaphrodites with 5-alpha-reductase deficiency in Papua New ology. T. and pseudohermaphroditic female rhesus monkeys. E. H. 289-308.. Sexual preferences in neona. 400-412). Brutpflege. H. pp. Psychoendocrine research on sexual natal testosterone treatment on defeminization of sexual receptivity orientation. G. R. Uylings. J. Australian finches in bush and aviary. (1984). M. 63. J. NEWMAN. 143. Psychoneuroendocrinology. 133-143). L. 659. 637-645. Cambridge. 52. B. Homwnes & Behavior. PETERSON. 11. Homosexual tity. 73-83. of the effect of estradiol benzoate. L. M. J. R. J. insensitivity syndrome compared. M. I. J... RAO.). M. Physiology & Behavior. Morges. Mating 00. In D. H. C.. R. 5. Physiology & Behavior. Psychoneuroendocrinology. L. & HALLMAN. & GOY. &STURLA. & FARNER.. C. R. W. J. & McEWEN... HERDT.). J. C. J. & CHRISTENSON.). R. J.). P. Oxford. 1. social behaviour ofthe Norway rat. C. D. (1967). 9. (1982). 167-176. A. M.). J. T. H. 384-399.XY androgen- und Tagesperiodik beim Europäischen Wildschwein (Sus scro/a L. J. J. Postnatal differentiation of sexual preference in ME\-NICK. J. KESTER. Uy. sickness. Sexual Behavior. 955-995.. B. pp. Maternal contributions to the development of Sociocultural and clinical aspects of gender formation in male pseu. De Bruin. Crews (Ed. 1173-1239).. & BAUM. A.. or status? Homosexual gender iden- transsexual subjects. Cercopithecines in multi- male pigs. R.. 25. Endocrine aspects of female-female pairing in the Western haviour of the golden hamster under seminatural conditions. STOCKMAN. estradiol and rnating experience. NJ: Prentice Hall. mone to estrogen administration in heterosexuaI. Sexual dimorphism and transsexuality: Clinical Press. Wrangham. & PEARL. GooREN. MEYERSON. J. LISK. Corner (Eds. R. (1980).. (1980). and MONEY. Cheney. YOUNG. J. & MEYERSON. J. Cheney. H. & WILLIAMS. 0/ Reproduction.. B. M. WINGFIELD. G. T. E. C. & MATTHEWS.. Chicago: Univer- 213-218. A. IMPERATo-McGINLEY.. (1987). Journal 0/ deficiency-a model for the role of androgens in both the develop. (1984). GREEN. SCHWARTZ. G. The hormones and mating OOhavior. 1988. & T. 160-164. (1986). F. (1988). Psychobiology 0/ reproductive behavior: An evolutionary perspective (pp. Male pseudohermaphroditism secondary to 5a-reductase SIGNORET. 212-218. C. VAN KESSEL. M. homosexuaI. Reproduction & Fertility (Suppl. POMERANTZ. Animal gull (Larus occidentalis wymam). D... (1987). biosciences (Vol. (1978).). L. C.. observations. T. 61. GAUnER. (1984). Zeitschrift für Tierpsychologie. J. Oe Vries. (1986). C. 405-414. FINCH. (1983b). Sex-specific orien- IUCN. 174.and post. 11. Primate societies (pp. 39-69. M. 1-80. (1983). Sex and internal secretions (Vol. K. 399-4(6). W. A. ANIMAL SEXUAL ORIENT AnON 347 FORD.666. & M. (1964). L. 41. R. Journal 0/ Clinical Endocrinology & Metabolism. E. pp.. Amsterdam: Elsevier. A. K. & TIEFER. J. Adult erotosex- brain. R. 35. W. Guinea. B. Quarterly Review 409-414. L. H. Monogamy in mammals. D. En- glewood Cliffs. D.XX congenital virilizing adrenal hyperplasia and 46. Influences ofpre.!CHARD. L. & M. 9. 30. B. H. (1985). YOUNG. B. Kaye (Eds. G. & CARANZARO. H. 121-134).. SLOB. Journal 0/ Steroid Biochemistry. Prena. 389). Sex differences in the brain: Progress the female rat: A methodological study applied to the investigation in brain research (Vol. Sexual competition and mate choice. A. Trends in Neurosciences. EUASSON. C. CIACCIO. R. 176-203). S. K. Primates in Nature. J. In G. J. A. (1970). Sex FRÄDRICH. J. L. and heterosexual partner preference in ovariectornized female rats: JAMIESON. & BAUM. HETTA. 451-460). sity of Chicago Press. R.. development in male pigs. C. Walther (Eds. 31. ment 0/ responsiveness to steroid homwnes: Advances in the 1496-1500. Sexual motivation in the male (1985). Smuts. Reproductive behaviour of pigs.. 878-889... J. Geist & F. T. & DAVIDSON.. R. Physiology courtship and copulation behaviour in a communally breeding bird. Science. choneuroendocrinology. (1983a). 152-162. (1984). 375- V. Effects tal 'female hormone' administration and psychosexual development of neonatal castration and testosterone propionate treatment on sex- in human males. A functional approach to the OOhavioraI and sexual behavior. J. In W. 225. 581-587. 42. J.