AMER. ZOOL.. 18:501-509 (1978).
Sex Steroids and the Differentiation of Avian Reproductive Behavior
ELIZABETH KOCHER ADKINS
Department of Psychology and Section of Neurobiology and Behavior,
Cornell University, Ithaca, New York 14853
SYNOPSIS Experiments in which avian embryos are treated with sex steroids or steroid
antagonists suggest that sexual differentiation of reproductive behavior (and thus differentiation of the brain mechanisms for such behavior) is controlled by steroids produced
by the embryonic gonads. In chickens and Japanese quail, males hatched from eggs treated
with estradiol or testosterone during incubation are feminized (demasculinized); they fail
to exhibit masculine sexual behavior as adults, and no longer are behaviorally distinguishable from females. Some evidence suggests that testosterone may mimic the feminizing
action of estradiol by being converted to an estrogen in the embryonic brain. Genetic
female quail exposed to an antiestrogen during embryonic development are masculinized;
they exhibit an increased ability to display the masculine copulatory pattern. Thus the
behavior of these species is feminized by embryonic exposure to sex steroids, the
anhormonal (neutral) sex for behavioral differentiation appears to be the male, and
females appear to result from estrogen produced by the embryonic ovaries. In contrast,
sex steroid treatment of mammals early in development masculinizes behavior, the female
is the neutral sex, and males result from fetal androgen secretion. These opposite patterns
of psychosexual differentiation in birds and mammals are correlated with a major
difference between the avian and mammalian sex-determining mechanism. Implications
for other vertebrates are discussed.
INTRODUCTION
Sexual dimorphism has a long and illustrious history of study in zoology. In recent
years, behavioral dimorphism (sexual
diethism—Shepard, 1975) has received
increasing attention. Whether the focus is
on behavior or morphology, a question of
primary importance is, what are the developmental origins of these sex differences? Obviously the ultimate source is the
sex chromosomes, but what is the actual
mechanism by which adult sex differences
are produced?
BEHAVIORAL DIFFERENTIATION IN MAMMALS
In this paper I would like to review the
current state of knowledge about the developmental origins of sexual diethism in
birds. To accomplish this, it will first be
necessary to briefly review the relevant
The author's experiments described herein were
supported by P.H.S. grant MH-21435 and N.S.F.
grant BNS76-24308. Address reprint requests to E.
Adkins, Department of Psychology, Uris Hall, Cornell University, Ithaca, NY 14853.
mammalian literature, since much of the
avian research is modeled on work with
mammals. Quite different results are obtained, however. In the mammalian research, interest has focused chiefly on
diethism in copulatory behavior per se,
especially in laboratory rodents—on the
fact that male mammals typically mount,
thrust, and intromit the penis during mating, whereas females typically adopt some
very different postures such as lordosis,
the concave-back position of the receptive
female rodent. These behavior patterns
are under the control of gonadal steroids,
and thus an obvious source of the sex
difference in copulatory behavior is
gonadal dimorphism. During copulation,
males are being exposed primarily to circulating androgens, whereas females are
being exposed primarily to circulating estrogens and progestagens. If gonadal dimorphism were the sole source of this
diethism, then if males and females were to
be exposed to the same hormones and the
same stimuli during mating, the sex difference should disappear. This is not the
case. To take the laboratory rat as an
example, if adult rats of both sexes are
501
502
ELIZABETH KOCHER ADKINS
gonadectomized, treated with the same
dosage of testosterone, and placed with
sexually active female partners, the
testosterone-treated females will exhibit
surprisingly high levels of mounting and
intromission, but the males will exhibit
even higher levels, and will be more likely
to exhibit the complete mating pattern
(Pfaff, 1970; Young, 1961). If adults of
both sexes are gonadectomized, treated
with identical dosages of estrogen and
progesterone, and placed with sexually active male partners, the females will readily
adopt the lordosis posture in response to
the partner's copulatory attempts, whereas
the hormone-treated males will adopt this
posture only rarely (Pfaff, 1970; Young,
1961). Therefore each sex seems to have
the neural capacity for both masculine and
feminine mating patterns, and thus is fundamentally behaviorally bisexual; their
nervous systems, however, are dimorphic
with respect to the ease with which these
mating patterns can be activated by sex
hormones. Males are more responsive than
females in terms of the hormonal activation of mounting and intromission,
whereas females are quite a bit more responsive than males in terms of the hormonal activation of the loidosis posture.
Thus both neural and gonadal dimorphism account for the diethism seen in normal intact animals.
T h e developmental origins of this
neural dimorphism lie in the secretions of
the fetal and early postnatal gonads. In the
laboratory rat, the presence of neonatal
androgens during a critical period results
in the development of the masculine pattern of hormone responsiveness, whereas
the absence of androgens at this time results in the feminine pattern of hormone
responsiveness (Feeler and Wade, 1974;
Whalen, 1968; Young, 1965). Genetic
females treated with testosterone shortly
after birth are permanently masculinized;
as adults they will respond to testosterone
by showing high levels of mounting and
intromission, and will respond to estrogen
and progesterone by showing only low
levels of lordosis. Genetic males castrated
before differentiation has taken place will
be permanent!) feminized; as adults the\
will show good lordosis in response to
estrogen and progesterone, and show reduced levels of mounting and intromission
in response to testosterone. Females
gonadectomized before differentiation are
unaffected; the ovaries are not necessary
for feminine behavioral development.
A similar pattern of results, in which
early treatment with testosterone masculinizes females and early castration
feminizes males, has been observed in several other mammalian species, including
hamsters (Mesocricetus auratus) (Clemens,
1974), guinea pigs (Cavia porcellus)
(Phoenix et al., 1959), mice (Mus musculw)
(Edwards and Burge, 1971), dogs (Canis
fnmiliaris) (Beach, 1975), ferrets (Mustela
furo) (Baum, 1976), and rhesus monkeys
(Macaco, mulatta) (Goy, 1970).
Several important conclusions emerge
from these studies of psychosexual differentiation in mammals. First, the sex
chromosomes act indirectly, via their effect
on gonad differentiation, to determine
sexual diethism in copulation. Second, sex
hormones alter the course of brain differentiation during limited critical periods.
Third, mammalian psychosexual differentiation follows a pattern in which females
result from an absence of androgen during
development, and males result from the
presence of androgen. Since animals
gonadectomized before differentiation
develop as behavioral females, regardless
of genetic sex, the female is the anhormonal (neutral) sex. This pattern parallels
nicely sexual differentiation of morphological characters in mammals (Burns,
1961 ;Bruner-Lorand, 1964).
BEHAVIORAL DIFFERENTIATION IN BIRDS
To date, most experiments on the role of
sex steroids in psychosexual differentiation have used mammals as subjects; yet
for some purposes birds are more suitable.
Several of the common domestic species,
poultry in particular, are considerably
more dimorphic than are laboratory
mammals. In addition, avian reproductive
behavior is primarily mediated by visual
and auditory modalities, and thus is accessible to human observers; whereas mam-
AVIAN PSYCHOSEXUAL DIFFERENTIATION
503
malian reproductive behavior is often neural differentiation has actually been alhighly olfactory. This is particularly true of tered. In all cases, the birds were observed
courtship, which in many birds is richly in the intact state, and there is no guaranexpressed in a manner that can easily be tee that the males had sufficient circulating
measured and recorded. Treatment of androgen at the time of testing to activate
mammals during embryonic development behavior. In fact, treatment of eggs with
can seriously interfere with gestation, and steroids is known to impair the developeffects are confounded by alterations in ment of the testes (Glick, 1961; Pantic and
the mother's hormones. These problems Kosanovic, 1973; Wentworth et al., 1968).
are not encountered in avian research.
The most important reason for studying Differentiation of behavior in chickens
birds, however, is that very different results are obtained that shed light on the
Chickens are one of two avian species at
evolution of sex differentiation in verte- this time for which we do have more conbrates. I n those avian species that have been clusive evidence that embryonic exposure
studied thus far, early treatment with sex to sex steroids alters behavioral and brain
steroids feminizes behavior, rather than differentiation. This evidence is a study by
masculinizing it.
Wilson and Glick (1970). In their experiFor years, attempts have been made to ments, chicken eggs were either dipped in
alter the sex of birds or to sterilize them by solutions of testosterone propionate or
treating incubating eggs with sex steroids, estradiol-17/3 benzoate after three clays of
and in some experiments, observations of incubation, or were injected with these
behavior suggested that such treatment steroids on different days of incubation.
had dramatic effects on adult mating. For Sexual behavior was activated precociously
example, Domm (1939) injected eggs of by injecting juveniles with testosterone
domestic chickens (Gallus gallus) with sev- propionate and testing them at 41 to 49
eral estrogens between the third and fifth days of age posthatching. Treatment with
days of incubation. When the birds either steroid prior to day 13 of incubation
reached adulthood and were observed in greatly suppressed the frequency of atsocial groups, the males with the most tempted matings by males. Masculine matfeminized plumage rarely copulated, ing attempts by females were also supwhereas the females were behaviorally pressed. Waltzing, a masculine courtship and
normal. More recent experiments contain threat display, was reduced in frequency,
similar observations. Kaufman (1956) in- but not to as great an extent as mating.
jected rutoestrol into chicken eggs after 24 These effects were not seen if treatment
or 48 hours of incubation. The males that occurred on or after day 13. In contrast,
hatched from these eggs never crowed or treated females showed normal receptive
copulated. Click (1961, 1965) dipped chic- behavior as adults; feminine behavior was
ken eggs in solutions of testosterone pro- not affected. Thus either testosterone or
pionate after 3 days of incubation, and estradiol feminizes male chickens (or more
males hatched from these eggs failed to accurately, demasculinizes them) by supmate as adults. Male Japanese quail pressing masculine behavioral potential
(domesticated Coturnix colurnix japonica) without interfering with feminine behavhatched from eggs sprayed with mestranol ioral potential. This demasculinization is
on clay 0, 6, or 12 of incubation also were limited to a critical period prior to hatching
deficient in copulation (Wentworth el al., in this precocial species.
1968). Pigeons (Columba livid) implanted
with subcutaneous pellets of diethylstilbestrol just after hatching showed reduced Differentiation of behavior in quail; quail and
levels of nest-calling and bow-cooing (mas- chickens compared
culine behavior patterns) (Orcutt, 1971).
For the last 6 years, I have been conductNone of these experiments, however, proing
a research program on the role of sex
vide conclusive evidence that behavioral or
steroids in the psychosexual differentia-
504
ELIZABETH KOCHER ADKINS
tion of Japanese quail. This species is well
suited to this type of research. Maturation
is rapid (about 5 to 6 weeks from hatching
to sexual maturity), and the birds are
small, lay large numbers of eggs, and are
quite active with respect to sexual behavior. Like chickens, Japanese quail
exhibit marked sexual cliethism (see Adkins and Adler, 1972, Sachs, 1969, and
Wilson and Bermant, 1972, for a fuller
description of the behavior of this species).
Males crow, especially when unmated or
separated from females, whereas females
under these conditions emit a call resembling cricket song (Potash, 1975). Males may
strut either before or after copulation.
Copulation occurs as follows. The female
may solicit mating by rubbing against the
male's breast or gently pecking him. The
male grabs the feathers of the female's
head or neck, mounts, and then spreads
his wings and leans back so as to press his
cloaca against hers. During copulation the
female squats and refrains from locomoting. After a brief cloacal contact, the male
dismounts and may strut.
Experiments in which adult quail are
exposed to a short photoperiod, which
causes pronounced gonadal regression,
and treated with sex steroids indicate that
females treated with testosterone and
tested with receptive female partners crow
and strut (though not as frequently as
males), but very rarely perform the head
grab — mount — cloacal contact movement sequence; whereas males treated
with estradiol and tested with male
partners readily squat and permit copulation (Adkins, 1975; Adkins and Adler,
1972). These males do not differ either
quantitatively or qualitatively from females
treated with the same dosage of estradiol.
Thus in this species, the sex difference
seen in intact birds in the display of
feminine sexual receptivity seems to be
due largely to gonadal dimorphism at the
time of testing; there does not seem to be
any underlying neural dimorphism. In
contrast, the masculine copulatory pattern
is very difficult to activate in females, and
the sex difference seen in intact birds in
this behavior seems to be due to neural
dimorphism. Thus the fundamental sex
difference in quail sexual behavior lies in
the capacity to display the masculine
copulatory sequence.
What effect does sex steroid treatment
during early development have on the
differentiation of these behavior patterns?
In quail, as in chickens, sex steroids
primarily feminize (demasculinize) males
(Adkins, 1975). In this experiment, eggs of
quail were injected with 0.05 mg
estradiol-17/3 benzoate or with 2.5 or 1.2
mg testosterone propionate on the tenth
day of incubation. Upon reaching maturity, all birds were exposed to a short
photoperiod to eliminate endogenous
gonadal hormones. They were then either
injected with estradiol benzoate for 9 to 11
days and tested with male partners for
display of feminine behavior, or were injected with testosterone for 9 to 11 clays
and tested with female partners for display
of masculine behavior. The results for
masculine behavior patterns are shown in
Table 1. Note first the diethism seen in the
control males and females, who differed
markedly in their ability to exhibit the
complete masculine copulatory sequence.
The major result summarized in Table 1
was that either estradiol or testosterone
injected into the eggs greatly suppressed
the capacity of males to display the head
grab—mount—cloacal contact movement
sequence. Crowing and strutting were also
suppressed, but this suppression was not as
significant due to the lower control levels.
Testosterone did not increase the ability of
females to display masculine behavior; i.e.,
the females were not masculinized. When
birds were tested with male partners following estradiol replacement, there were
no effects of the egg treatments on
feminine sexual receptivity in either sex.
This result was expected, given that there
seems to be little difference between the
sexes in the ability to display this behavior.
The results of this experiment can be
summarized by stating that the sex difference in masculine behavior seen in normal
untreated quail is eliminated by treatment
of eggs with sex steroids. Treated females
are unchanged, but treated males are
turned into behavioral females. Additional
data showing that either estradiol or testos-
505
AVIAN KSYCHOSEXUAI. DIFFERENTIATION
TAB1.K I. Masculine sexual behavior nj Japanese quail hatched from eggs injected with estradiol bntzimle (EH) or
testosterone propionate (IP) on day 10 o)'incubation."
Number of birds
Sex
Males
Kgg treatment
None
Vehicle
KB
TP
Females
None
Vehicle
KB
'IT
N
Copulating'1
Crowing
Sirutiing
10
10
10
10
6
7
0"
ld
6
(i
(i
()d
2
10
10
4
10
0
0
0
y
0
0
1
1
0
0
4
9
0
0
a
Data are from Adkins (1975). Dosages were 0.05 nig KB and 2.5 or 1.2 mg TP. All birds were tested with
sexually-active female partners after being exposed to a short pholoperiod for 3 weeks and then in)ecte<l with
TP for 9 to 11 clays.
h
I. e., exhibiting the sequence head grab—mount—cloacal contact movement.
c
These females performed the head grab only; they did not mounl.
d
P < .05 compared wilh vehicle group.
terone demasculinize male quail have been
obtained in another laboratory (Whitsett e/
al., 1977).
In the experiment described above (Adkins, 1975) the dosages used to demasculinize males were quite large. Subsequent experiments show that the same
effect can be produced with much smaller
dosages that are probably in the physiological range. Whitsett el al. (1977) found that
as little as 2 fig estradiol-17/3 injected into
eggs significantly lowered head grabbing
and mounting frequencies. Adkins (unpublished data) found that I /u,g
estracliol-17/3 benzoate was still sufficient
to significantly lower the percentage of
males displaying the head grab —
mount—cloacal contact movement sequence. Testosterone is not as effective as
estradiol at the same dosage (Whitsett el al.,
1977); the minimum effective dosage of
testosterone propionate is about 100 /Mg
(Adkins, unpublished data).
In chickens, which have a 2 1 day incubation period, treatment of eggs with estradiol or testosterone prior to day 13
demasculinizes males. In Japanese quail,
which have an 18 day incubation period in
the author's laboratory, treatment with estradiol prior to but not after day 12 demasculinizes males, and treatment on day 12 is
partially, but not significantly, effective
(see Figure 1). Thus in both of these highly
precocial species, the critical period for
sexual differentiation of the brain ends
before hatching.
Figure 1 also shows the effect of treatment wilh estradiol on different clays of
incubation on the proctodeal (foam) gland
development of males. The prod odea I
gland, unique to the genus Coliinux, is
sexually dimorphic; in untreated adults it
<
Q
BEHAVIOR
H
GLANDS
50 .
a.
o
o
XI
OIL
(10)
rn
EB-IO
(9)
m
•>
EB-II
(10)
EB-12
(81
EB-13
(10)
EB-14
(II)
EGG TREATMENT - DAY
J"
FIG. I Masculine copulalory behavior and proctodeal gland development of male Japanese quail
hatched from eggs injected with 0.05 mg estradiol
benzoate (KB) on day 10, II, 12, 13, or 14 of
incubation or with the oil vehicle on day 10 (Adkins,
unpublished data). All males had photically-regrcssed
testes and were receiving daily injections of testosterone when tested with female partners. Numbers in
parentheses are .Vs. *P < .05 compared with oiltreated group.
ELIZABETH KOCHER ADKINS
506
is well developed only in the male. It is
androgen-dependent, regresses following
castration (Sachs, 1969), and is demasculinized b)r embryonic exposure to estradiol or testosterone (Adkins, 1975).
Thus in two species of birds, embryonic
exposure to sex steroids demasculinizes
males, rather than masculinizing females.
By analogy with mammalian sexual differentiation, these results suggest that the
male is the neutral (anhormonal) sex and
that ovarian estrogen induces feminine
behavioral development. More direct evidence for this pattern of sexual differentiation could be obtained by studying birds
gonadectomized prior to differentiation.
At the present time, this is not technically
possible in either chickens or quail, but can
be functionally accomplished by administering antihormones. If embryonic ovarian
estrogen overcomes the neutral male pattern to induce females, then genetic
females exposed to an antiestrogen should
fail to be feminized, and should show behavioral masculinization. Such a result has
been obtained in quail, using the chemical
antiestrogen CI-628 (Adkins, 1976), and is
summarized in Figure 2. Males hatched
en
—
<
from eggs injected on day 9 of incubation
with 0.1 mg CI-628 were unaffected. Control females, as expected, never performed
the complete masculine copulatory sequence (head grab — mount — cloacal
contact movement). Females hatched from
eggs injected on day 9 with 0.1 mg CI-628,
on the other hand, were behaviorally masculinized. A few actually performed the
complete male mating pattern, and qualitatively they resembled males. This experiment suggests that the male quail is the
neutral sex for behavioral differentiation.
The theory that the male is the neutral
sex in chickens and quail and that female
differentiation is induced by embryonic
ovarian estrogen receives additional support from data on morphological and
neurobiological development during embryonic life. In both species, morphological differentiation follows a pattern in
which the male is the neutral sex and
ovarian hormones suppress development
of male characters in genetic females
(Burns, 1961;Taber, 1964). The ovaries of
chicken and quail embryos are actively
engaged in steroidogenesis, and produce
significant quantities of estrogens
(Guichard el a!., 1977; Haffen, 1975;
Ozon, 1965). Functional estradiol receptors appear to be present in the
IOO
D
HEAD GRAB
x
H
MOUNT
LJ
CD
SCCM
t50
50Q_
CD
O
O
X
X
LJ
0 OIL
WATER (4)
C I - 6 2 8 (91
MALES
EGG
WATERI9I
CI-62819)
FEMALES
TREATMENT
FIG. 2. Masculine copulatory behavior exhibited by
male and female Japanese quail hatched from eggs
injected on day 9 of incubalion with 0.1 mg CI-628 or
with the distilled water vehicle. Data are from Adkins
(1976). CCM —cloacal contact movement. All birds
had photicall)-regressed gonads and were receiving
dail) injections of testosterone when tested with
female partners. Numbers in parentheses are X's.
': P < ().."> compared with w.iter-treatt'd females.
(10)
TP-IMG
(II)
TP-2MG DP-1 MG DP-2MG
(10)
(8)
(8)
EGG TREATMENT
FIG. 3. Masculine copulatory behavior of male
Japanese quail hatched from eggs injected on day 10
of incubation with I or 2 mg testosterone propionate
(TP), with 1 or 2 mg dihydrotestosterone propionate
(DP), or with the oil vehicle (Adkins and Pickett,
unpublished data). All birds had photically-regressed
testes and were receiving dail) injections of testosterone propionate when tested with female partners.
Numbers in parentheses are N's. * P < .05 vjompared
with oil-treated group.
AVIAN PSYCHOSEXUAL DIFFERENTIATION
507
hypothalamus of the brain of the chick male chickens but not of males from
embryo as early as day 10 (Martinez- testosterone-treated eggs, indicating that
embryonic exposure to testosterone does
Vargas et al., 1975).
not suppress mating behavior by making
the red nuclei more inhibitory than normal
MECHANISMS OF AVIAN PSYCHOSEXUAL
(Crawford and Glick, 1975).'
DIFFERENTIATION
What are the neural and biochemical COMPARATIVE PERSPECTIVES ON PSVCHOSEXLAI.
mechanisms by which sex steroids feminize
DIFFERENTIATION
the brains of chickens and quail? Some
clues to the biochemical mechanisms can
In addition to asking reductionistic
be obtained by comparing the actions of analytical questions about psychosexual
several different steroids. Whitsett et al. differentiation, it is important to ask com(1977) found that treatment of eggs with 2 parative synthetic questions. Is the pattern
fxg of each of the following estrogens sig- of differentiation found in chickens and
nificantly reduced subsequent mounting quail a characteristic of the class Aves in
by male quail: estradiol-17/3, estradiol-17a, general? Studies of other species are sorely
estriol, estrone, diethylstilbestrol. It is lacking but vitally important. Experiments
especially interesting that testosterone also on morphological differentiation in
feminizes sexual behavior (Adkins, 1975; domestic ducks (Anas platyrhynchos) suggest
Whitsett <'t al., 1977). A possible reason for that their behavioral differentiation will
this paradoxical effect is that testosterone resemble the chicken/quail pattern (Wolff,
is converted to an estrogen in the embry- 1959).
onic brain, as seems to occur in the differIf the male is generally the neutral sex in
entiating rat brain (Weiszand Gibbs, 1974), birds, why do birds and mammals difand in fact there is already some evidence ferentiate in such opposite ways? The conthat this is the case. Dihydrotestosterone, trasting patterns of sex differentiation in
which is not known to undergo conversion birds and mammals may be related to the
to estrogen in vertebrates (Idler, 1972), fact that mammals, but not birds, have
fails to feminize male quail. As shown in internal gestation. Both Burns (1961) and
Figure .S, even when it is injected into eggs Mittwoch (1975) have pointed out that if
at high dosages, it has absolutely no effect male mammals were the neutral sex, they
on the differentiation of the masculine would risk being feminized by the mother's
mating pattern (Adkins and Picketl, un- hormones. In addition, the contrasting
published data). In addition, the brain of bird and mammal patterns are clearly
the chick has been shown to contain sig- closely tied to another major difference
nificant quantities of aromatase, the en- between avian and mammalian sex — the
zyme responsible for converting andro- fact that in mammals, the female is the
gens to estrogens (Callard et al., 1978).
homogametic sex (the one with two similar
Glick and his colleagues have explored sex chromosomes, referred to as XX),
several possible mechanisms by which sex whereas in birds, the male is always the
steroids could demasculinize the em- homogametic sex (Beatty, 1964). Thus in
bryonic chicken brain. Wilson and Glick both classes the homogametic sex is the
(1970) found that chicks hatched from neutral sex. This correlation between sex
eggs clipped in testosterone on incubation determination and sex differentiation has
day 3, 6, or 12, but not 18, had reduced been noted previously with reference to
levels of cholesterol in the cerebral hemi- morphological development (Burns, 1961;
spheres. Ghicks from eggs dipped in testos- Van Tienhoven, 1968; Witschi, 1959); it
terone on day 3 had reduced levels of now appears that it can be extended to
alkaline phosphatase activity in the brain behavioral differentiation as well.
stem (Kilgore and Glick, 1970). Lesions of
There are suggestions that this principle
the red nuclei (midbrain structures) in- that the homogametic sex is the neutral sex
creased the mating behavior of normal may apply to other vertebrates as well.
ELIZABETH KOCHER ADKINS
508
Unfortunately, little or no information is
available concerning behavioral differentiation in other classes, and so one has to rely
on what is known about morphological
differentiation (see Adkins, 1978, for a
detailed review of sexual differentiation in
non-mammalian vertebrates and for references for the following summary). The
male lizard Lnrcrla vivipara is homogametic
and is the morphological neutral sex. In
the u r o d e l e a m p h i b i a n s Ambystoma
mrxiramim
a n d Plcurodclcs waltlii, a n d i n t h e
a n u r a n Xetiopus laevis, the male is
homogametic and embryos are strongly
feminized by treatment with sex steroids.
In the anurans Psrudacris nigrila and three
Raua species, the female is homogametic
and embryos are strongly masculinized by
treatment with sex steroids. Finally, most
fish studied to date have
female
homogamety, and sex steroids strongly
masculinize the fry of these species.
CONCLUSIONS
Of the two species of birds (chickens and
Japanese quail) that have been studied in
detail, both undergo psychosexual differentiation by a process in which the male
is the neutral sex and the ovaries induce
feminine development. This pattern
stands in marked contrast to psychosexual
differentiation in mammals, in which the
female is the neutral sex and the testes
induce masculine development. These
contrasting patterns parallel morphological differentiation and are correlated with
a major difference between the two classes
in the genetic sex-determining mechanism.
In both cases ihe homogametic sex is the
neutral sex. Avian studies of psychosexual
differentiation demonstrate the critical
importance of a comparative approach to
the study of the role of sex steroids in brain
differentiation. Such an approach can
suggest evolutionary principles that would
otherwise go undetected.
REFERENCES
Adkins. E. K. 1975. Hormonal basis of sexu.il diffeienliation in [he Japanese quail. J. Comp. Phvsiol.
Psychol. 89:61-71."
Adkins, K. K. H)7C>. Enibnonk exposuie to an antics-
trogen masculinizes behavior of female quail.
Physiol. Behav. 17:357-359.
Adkins, E. K. 1978. Early organizational effects of
hormones: An evolutionary perspective. In X. T.
Adler (ed.), A primer of neuroendoenne function and
behavior. Plenum Press, New York. (In press)
Adkins, E. K. and N. T. Adler. 1972. Hormonal
control of behavior in the Japanese quail. J. Comp.
Physiol. Psychol. 81:27-36.
Baum, M.J. 1976. Effects of testosterone propionate
administered perinatally on sexual behavior of
female ferrets. J. Comp. Physiol. Psychol. 90:399410.
Beach, F. A. 1975. Hormonal modification of sexually
dimorphic behavior. Psychoneuroendocnnology
1:3-24.
Beally, R. A. 1964. Chromosome deviations and sex
in vertebrates. In C. N. Armstrong and A. J. Marshall (eds.), Intersexuality in vertebrates including man.
pp. 17-144. Academic Press, London.
Bruner-l.orand, ). 1964. Intersexuality in mammals.
In C. N. Armstrong and A. J. Marshall (eds),
Intersexuality
in vertebrates
including
man, p p . 3 1 1 -
348. Academic Press, London.
Burns, R. K. 1961. Role of hormones in the differentiation of sex. In W. C. Young (ed.), Sex and internal
secretions. Vol. 1, pp. 76-160. Williams and Wilkins,
Baltimore.
Callard, G. V., Z. Petro, and K. J. Ryan. 1978.
Conversion ol androgen to estrogen and other
steroids in the vertebrate brain. Amer. Zool.
18:511-523.
Clemens, L. G. 1974. Neurohormonal control of male
sexual behavior. In W. Montagna and W. A. Sadler
(eds.), Reproductive behavior, pp. 23-54. Plenum
Press, New York.
Crawford, W. C. and B. Click. 1975 The function of
preoptic, mammilaris lateralis and ruber nuclei in
normal and sexually inactive male chickens.
Physiol. Behav. 15:171-176.
Domm, L. V. 1939. Intersexuality in adult Brown
Leghorn males as a result of estrogenic treatment
during early embryonic life. Proc. Soc. Exp. Biol.
Med. 42:3 10-3 12.
Edwards, I). A. and K. G. Bulge. 1971. Early androgen treatment and male and female sexual behavior in mice. Horm. Behav. 2:49-58.
Feeler, H. H. and G. X. Wade. 1974. Integrative
ailions of petinatal hormones on neural tissues
mediating adult sexual behavioi. In F. O. Schmitt
and F. G. Worden (eds.). The neunnciences- Third
itudy progtam, pp. 583-586. MIT Press, Cambridge,
Mass.
Click, B. 1961. The reproductive performance of
birds hatched from eggs dipped in male hormone
solutions. Poultry Sci. 40:1408. (Abstr.)
Click, B. 1965. Embryonic exposure to testosterone
propionatc will adversely influence future mating
behavior in male chickens. Fed. Proc. 24:700.
(Abstr.)
Goy, R. VV. 1970. Experimental control of psychosexuality. Phil. Trans. Roy. Soc. London B. 259:149162.'
Guichard, A., 1.. Cedard, Th.-M. Mignot, D. Scheib,
and K. Haflen. 11)77. Radioimmunoassav ol
AVIAN PSYCHOSEXUAL DIFFERENTIATION
steroids produced by cultured chick embryonic
gonads: Differences according to age, sex, and side.
Gen. Comp. Endocr. 32:255-265.
Haffen, K. 1975. Sex differentiation of avian gonads
in vitro. Amer. Zool. 15:257-272.
Idler. D. R. (ed.) 1972. Steroids in nonmammalian
vertebrates. Academic Press, New York.
Kaufman, L. 1956. Experiments on sex modification
in cocks during their embryonal development.
World's Poultry Sci. J. 12:41. (Abstr.)
Kilgore, L. and B. Click. 1970. Testosterone's
influence on brain enzymes in the developing chick.
Poultry Sci. 49:16-22.
Martinez-Vargas, M. C , D. B. Gibson, M. Sar, and W.
E. Stumpf. 1975. Estrogen target sites in the brain
of the chick embryo. Science 190:1307-1309.
Mittwoch, U. 1975. Chromosomes and sex differentiation. In R. Reinboth (ed.), Intersexuality in the animal
kingdom, pp. 438-446. Springer-Verlag, New York.
Orcutt, F. S. 1971. Effects of oestrogen on the differentiation of some reproductive behaviours in
male pigeons (Columba livia). Anim. Behav.
19.277-286.
Ozon, R. 1965. Mise en evidence d'hormones
steroides oestrogenes dans le sang de la poule
adulte et chez I'embryon de poulet. C. R. Acad. Sci.
261:5664-5666.
Pantic, V. R. and M. V. Kosanovic. 1973. Testes of
roosters treated with a single dose of estradiol
dipropionate. Gen. Comp. Endocr. 21:108-117.
Pfaff, D. 1970. Nature of sex hormone effects on rat
sex behavior: Specificity of effects and individual
patterns of response. J. Comp. Physiol. Psychol.
73:349-358.
Phoenix, C. H., R. W. Goy, A. A. Gerall, and W. C.
Young. 1959. Organizing action of prenatally administered testosterone propionate on the tissues
mediating mating behavior in the female guinea
pig. Endocrinology 65:369-382.
Potash, L. M. 1975. An experimental analysis of the
use of location calls by Japanese quail, Coturnix
coturnixjaponica. Behaviour 54:153-180.
Sachs, B. D. 1969. Photoperiodic control of reproductive behavior and physiology of the male Japanese
quail (Coturnix roturnix japonica). Horm. Behav.
1:7-24.
Shepard, J. M. 1975. Factors influencing female
509
choice in the lek mating system of the ruff. Living
Bird 14:87-112.
Taber, E. 1964. Intersexuality in birds. In C. N.
Armstrong and A. J. Marshall (eds.), Interseximlity in
vertebrates including man, pp. 285-310. Academic
Press, London.
Van Tienhoven, A. 1968. Reproductive physiology of
vertebrates. Saunders, Philadelphia.
Weisz, J. and C. Gibbs. 1974. Metabolites of testosterone in the brain of the newborn female rat after
an injection of tritiated testosterone. Neuroendocrinology 14:72-86.
Wentworth, B. C, B. G. Hendricks. and J. Sturtevant.
1968. Sterility induced in Japanese quail by spray
treatment of eggs with mestranol. J. Wildl. Man.
32:879-887.
Whalen, R. E. 1968. Differentiation of the neural
mechanisms which control gonadotropin secretion
and sexual behavior. In M. Diamond (ed.), Perspectives in reproduction and sexual behavior, pp. 303-340.
Indiana U. Press, Bloomington.
Whitsett, J. M., E. W. Irvin, F. W. Edens, and J. P.
Thaxton. 1977. Demasculinization of male
Japanese quail by prenatal estrogen treatment.
Horm. Behav. 8:254-263.
Wilson, J. A. and B. Click. 1970. Ontogeny of mating
behavior in the chicken. Amer. J. Physiol.
218:951-955.
Wilson. M. I. and G. Bermant. 1972. An analysis of
social interactions in Japanese quail, Coturnix coturnix japonica. Anim. Behav. 20:252-258.
Witschi, E. 1959. Age of sex-determining mechanisms
in vertebrates. Science 130:372-375.
Wolff, E. 1959. Endocrine function of the gonad in
developing vertebrates. In A. Gorbman (ed.), Comparative endocrinology, pp. 568-581. Wiley, New
York.
Young, W. C. 1961. The hormones and mating
behavior. In W. C. Young (ed.). Sex and internal
secretions, Vol. 2, pp. 1173-1239. Williams and Wilkins, Baltimore.
Young. W. C. 1965. The organization of sexual
behavior by hormonal action during ihe prenatal
and larval periods in vertebrates. In F. A. Beach
(ed.), Sex and behavior, pp. 89-107. Wiley, New
York.