Women quail sex

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Edited by N. During embryonic development, gonadal steroid hormones androgens and estrogens are thought to organize the sexual differentiation of the brain in the heterogametic sexes of higher vertebrates males in mammals, females in birds. Brain differentiation of the homogametic sexes is thought to proceed by default, not requiring sex hormones for sex-specific organization.

In gallinaceous birds such as the Japanese quail, female brain organization is thought to develop via estrogen-dependent demasculinization of a default male brain phenotype. We performed male donor-to-female host MFfemale-to-male FMmale-to-male MMand female-to-female FF isotopic, isochronic transplantation of the forebrain primordium in Japanese quail embryos before gonadal differentiation had occurred; brain chimeras had a forebrain including the hypothalamus originating exclusively from donor cells. In contrast, FM chimeras genetically female forebrain, all other tissues genetically male showed no mounting and only rudimentary crowing behavior.

Although MM, FF, MF, and FM chimeras all showed host-typical production of steroid hormones during embryonic life, only FM chimeras were hypogonadal, had atypical low levels of circulating testosterone in adulthood, and showed reduction crowing or absence mounting of reproductive behaviors.

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Morphological features of the medial preoptic nucleus a sexually dimorphic brain area also were not male-like in FM males. These data demonstrate a brain-intrinsic, genetically determined component that organizes the sex-typical production of gonadal hormones in adulthood and call for a reevaluation of the mechanisms underlying brain sexual differentiation in other higher-vertebrate species.

Sexual differentiation of the brain and behavior of higher vertebrates is thought to be a stepwise process. In the current canonical model, a primary genetic program determines the development of the gonad. Gonadal sex determination le to sex-typical release of gonadal steroid hormones androgens and estrogens according to either a male or a female pattern.

Epigenetic action of androgens and estrogens then specifies the male or female differentiation of the brain, which is initially monomorphic 1 — 3. Gonad-hormone-dependent organization of brain sex occurs in birds and mammals in the heterogametic sex males in mammals, females in birdswhereas brain sex is thought to be default, not requiring gonadal hormones for sex-specific organization, in the homogametic sex 1 — 3.

Sex-specific phenotypes cannot be induced hormonally in adults of the opposite sex, whereas sex-typical phenotypes frequently are shown by only one sex but can occur spontaneously under certain physiological conditions and are hormone-inducible in adulthood in the opposite sex 5.

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To become overt, sexual phenotypes depend on the production of gonadal hormones via the hypothalamus—pituitary—gonad HPG axis in adulthood 4. The HPG axis also coordinates displays of sexual behavior with reproductive physiology. Sexual brain development therefore defines the ability of brain areas, including the neural part of the HPG axis, to respond to particular physiological als in adulthood 6.

Doubts about the adequacy of the canonical concept of gonadal hormone-dependent determination of brain sex and behavior have been raised by recent work on the vocal system of the zebra finch 7 — 9where partial sex reversal of the female gonad failed to induce a male-typical vocal control system 78. Other examples suggesting brain-intrinsic sex-determining mechanisms include the sexually dimorphic development of midbrain dopaminergic neurons of rodents in vitro 10 and incomplete sex-reversals of behavior after hormone treatments during early development 11 — These examples remain inconclusive because of the impossibility of exactly matching experimental procedures the exact dosage or timing of endocrine treatments used to modify the hormonal environment during brain development to individual variation in developmental processes.

Endocrine manipulations of embryonic development also are just as likely to act on the brain as they are on the gonad and other steroid-sensitive organs, making it difficult to disentangle the roles played by the brain and gonad during brain sexual differentiation. To circumvent these problems, this study used a nonendocrine manipulation involving the transfer of a male or female brain primordium to an undisturbed hormonal environment before the sexual differentiation of the gonad.

Male donor-to-female host MFfemale-to-male FMmale-to-male MMand female-to-female FF isotopic, isochronic transplantation of the brain primordium rostral to the otic capsules was performed on embryonic day 2 E2 in Japanese quails. In these brain chimeras, the forebrain including the hypothalamus originates from the donor 16 The primordia of the two other components of the HPG axis, Rathke's pouch adenopituitary and the gonadal anlage gonadare not transplanted and are of host origin.

Normal sexual differentiation in Japanese quail has been studied extensively 18 — 20 ; the gonadal anlage starts to produce estrogens around E6 in females only. These estrogens direct the undifferentiated gonad to form an ovary 18 Estrogen treatment of male quail embryos is demasculinizing, and inhibition of estrogen production of female embryos masculinizes their brain and behavior if treatments are before E14 Ovarian estrogen production thus is thought to demasculinize default male brain development in females.

If male brain development is default and female development occurs in the presence of ovarian hormones, then female brains in male bodies should develop into male brains and male brains in female bodies should develop into female brains host-typical development.

Although embryonic gonad formation and embryonic hormone production were normal in the brain chimeras studied here, gonadally male Japanese quails with female brains did not develop entirely male-like neural and behavioral phenotypes. Production of Chimeras.

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Japanese quail eggs were obtained from commercial sources and incubated within 24 h of laying in a forced-draft incubator at Experimental eggs were incubated for 36—45 h and transferred to small incubators in the operating room. The transplants were carried out between two quails as detailed ly for quail—chick chimeras 16 All surgical operations consisted of isochronic, isotopic transplants of the entire neural tube rostral to the otic capsules. Of all chimeras produced, 52 survived at least until E A total of 17 chimeras hatched successfully.

Fifteen of the hatched chimeras survived until posthatching day 50 for testing of adult sexual behavior. Sex Determination. Because the transplants were done without knowledge of the genetic sex of the eggs, postmortem sex determination to identify the genetic sex of the host and donor tissue was performed by using DNA techniques and following published protocols 18 For the animals killed between E11 and E13, the hypothalamic—preoptic area, the lower spinal cord, and the breast muscle were analyzed.

Each tissue of each animal yielded either male or female there were no mixed or ambiguous cases. Spinal cord and muscle tissue were always of the same genetic sex. The genetic sex of the hypothalamic—preoptic tissue of seven animals four FM and three MF differed from the spinal cord and breast muscles. This control experiment shows that the transplants performed always resulted in a genetically homogenous forebrain including the hypothalamus, as expected from quail—chicken chimeras 16 For the latter, we used the same procedure as above but replaced hypothalamic tissue with neostriatal tissue to allow morphometric analysis of the hypothalamus.

In seven cases, the neostriatal sex differed from the other tissues. From posthatching day 50 on, the chimeras and the control animals were housed individually in the same photoperiod. Vocalizations were recorded with a computer-based system during 3 h per day for 5 successive days. Animals were observed under these conditions for 1 h every second day for a period of 10 days. To test female sexual behavior, each chimera and control female were placed in the observation aviary together with an intact male for 1 h per day every second day for a period of 10 days.

Hormone Measurements. From the adult chimeras and six adult male and female controls, blood samples were taken from the wing vein before killing. From juvenile chimeras E11—E13 and six male E12 and six female E12 controls, blood samples were taken from the heart at killing. The intraassay variation was 5. PCR for Androgen Receptors. All subjects were administered lethal doses of isofluorane before perfusion. Subjects were perfused by intracardial perfusion with 0.

One series of sections was immunostained for aromatase, one for gonadotropin-releasing hormone I GnRH-Iand one for vasotocin under free-floating conditions, and then all were mounted on Superfrost slides. Immunostaining of aromatase, vasotocin, and GnRH-I followed published protocols employing the same antibodies 23 — Control staining using hypothalamic sections of other age-matched quails omitting the primary antibody resulted in no cell labeling.

The aromatase antibody was a gift from J. Hutchison Cambridge University, Cambridge, U. Sharp Roslin Institute, Edinburghand the vasotocin antibody was provided by E. Quantitative measurements of the sexually dimorphic nucleus of the quail preoptic area POM were done with a Leica Deerfield, IL microscope connected to a computer-based image-analysis system Imatec, Munich. Volume calculations of the POM were based on measurements of the area of each fifth section multiplied by the section thickness and intersection distance.

The extent of the POM on each section was calculated by manually tracing the area, following its boundary as indicated on the aromatase-stained sections. The subregion of the POM containing vasotocinergic fibers and cells was measured in the digitized sections adjacent to the aromatasestained sections as described First, the outlines of the POM were superimposed on the digitized vasotocin-immunostained section. Then, the fraction of the immunostained total surface of the POM was calculated. Data were checked for normality.

Unpaired t test was used for comparisons of the developmental data. Parametric ANOVA followed by Tukey's honestly ificant difference post hoc test was used for comparison of all adult data sets. Gonad Development and Hormone Production of the Chimeras. As detailed in Materials and Methodsall chimeras developed gon according to the genetic sex of the host. Hormone values were in the range ly published for quail embryos These data indicate normal autogenous production of gonadal steroids, indicating normal gonadal differentiation in chimeric embryos.

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PCR amplification of the androgen receptor in the brain primordium at the time of transplantation was negative. The ovary of the fourth MF chimera, which did not lay eggs, did not contain developed follicles at the time of killing. Similar letters indicate statistical similarity between these groups. Different letters indicate ificant differences between the groups. For statistical details, see the text.

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FM males differed from other males in testosterone production, POM volume, vasotocin staining in the POM, crowing activity, and mounting behavior. FM males differed from females in estradiol production, crowing activity, and receptivity. Brain Differentiation of the Chimeras. The POM is involved in the control of appetitive and consummatory e. The POM volume and of aromatase-containing neurons are sex-typical characteristics in adult, reproductively active quails 31 — Testosterone induces sexual dimorphism in both features in adulthood via its androgenic and estrogenic metabolites Because POM volume and the of aromatase-immunolabeled POM neurons were highly correlated, aromatase data were corrected for POM volume for group statistical comparisons.

Photomicrographs of coronal sections of the aromatase-stained POM arrowhe.

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All photomicrographs are taken at the level of the anterior commissure CA. Aromatase-stained neurons appear darkly. V, III ventricle. The density of vasotocinergic fibers and neurons has been interpreted as an organizational, sex-specific feature of the quail POM that becomes overt after elevated testosterone secretion in adult males Because POM size is positively correlated with the size of the subregion showing vasotocinergic staining, the latter were corrected for POM size for group statistical comparisons.

All other chimeras had vasotocinergic staining of the POM that was similar to controls of the same genetic sex. Anecdotally, the one MF chimera that showed low sexual activity see below had the strongest vasotocin immunostaining in the POM of all females including controls and FFs. GnRH-I is the main hypothalamic releasing factor that activates the adenopituitary in birds 2734 Behavioral Differentiation of the Chimeras.

Crowing is a testosterone-dependent, male-typical behavior; receptivity is an estrogen-dependent, female-typical behavior; and mounting is a testosterone-dependent, male-specific behavior The one MF female that did not lay eggs was the least receptive. The three FM males neither courted females nor showed mounting attempts Fig.

In summary, FM male, but not MF female, chimeras developed atypical sexual behavior. FM males showed neither male sex-specific behavior mounting nor female sex-typical behavior receptivity and only rudimentary sex-typical male behavior crowing. At the physiological level, FM chimeras differed from adult control and MM males in gonad weight, testosterone production, POM volume, the of aromatase-containing POM neurons, and the size of the vasotocinergic subregion of the POM.

Furthermore, FM chimeras differed from adult control, FF, and MF females because of the presence of testes and low estrogen production. The likely consequence of this hypogonadism of the FM males is that both testosterone- and estrogen-dependent, sex-typical phenotypes are lacking.

Whether the lack of sex-specific male phenotypes POM area of vasotocinergic structures, mounting of FM males from a difference in the developmental organization of the POM or a difference in the organization of the HPG axis see below that le to low adult testosterone production is unclear. The latter possibility is suggested by the more male-like vasotocinergic pattern of FM males compared with females, but this difference did not reach statistical ificance.

Women quail sex

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Differences Between Male and Female Quail