Glickman Stephen E, Short Roger V, Renfree Marilyn B
Department of Psychology, University of California, Berkeley, California 94720, USA.
Horm Behav. 2005 Nov;48(4):403-17. doi: 10.1016/j.yhbeh.2005.07.013. Epub 2005 Sep 28.
The present review explores sexual differentiation in three non-conventional species: the spotted hyena, the elephant and the tammar wallaby, selected because of the natural challenges they present for contemporary understanding of sexual differentiation. According to the prevailing view of mammalian sexual differentiation, originally proposed by Alfred Jost, secretion of androgen and anti-Mullerian hormone (AMH) by the fetal testes during critical stages of development accounts for the full range of sexually dimorphic urogenital traits observed at birth. Jost's concept was subsequently expanded to encompass sexual differentiation of the brain and behavior. Although the central focus of this review involves urogenital development, we assume that the novel mechanisms described in this article have potentially significant implications for sexual differentiation of brain and behavior, a transposition with precedent in the history of this field. Contrary to the "specific" requirements of Jost's formulation, female spotted hyenas and elephants initially develop male-type external genitalia prior to gonadal differentiation. In addition, the administration of anti-androgens to pregnant female spotted hyenas does not prevent the formation of a scrotum, pseudoscrotum, penis or penile clitoris in the offspring of treated females, although it is not yet clear whether the creation of masculine genitalia involves other steroids or whether there is a genetic mechanism bypassing a hormonal mediator. Wallabies, where sexual differentiation occurs in the pouch after birth, provide the most conclusive evidence for direct genetic control of sexual dimorphism, with the scrotum developing only in males and the pouch and mammary glands only in females, before differentiation of the gonads. The development of the pouch and mammary gland in females and the scrotum in males is controlled by genes on the X chromosome. In keeping with the "expanded" version of Jost's formulation, secretion of androgens by the fetal testes provides the best current account of a broad array of sex differences in reproductive morphology and endocrinology of the spotted hyena, and androgens are essential for development of the prostate and penis of the wallaby. But the essential circulating androgen in the male wallaby is 5alpha androstanediol, locally converted in target tissues to DHT, while in the pregnant female hyena, androstenedione, secreted by the maternal ovary, is converted by the placenta to testosterone (and estradiol) and transferred to the developing fetus. Testicular testosterone certainly seems to be responsible for the behavioral phenomenon of musth in male elephants. Both spotted hyenas and elephants display matrilineal social organization, and, in both species, female genital morphology requires feminine cooperation for successful copulation. We conclude that not all aspects of sexual differentiation have been delegated to testicular hormones in these mammals. In addition, we suggest that research on urogenital development in these non-traditional species directs attention to processes that may well be operating during the sexual differentiation of morphology and behavior in more common laboratory mammals, albeit in less dramatic fashion.
斑鬣狗、大象和帚尾袋鼩，选择它们是因为它们给当代性别分化的理解带来了自然挑战。根据阿尔弗雷德·约斯特最初提出的关于哺乳动物性别分化的主流观点，胎儿睾丸在发育关键阶段分泌雄激素和抗苗勒管激素（AMH），这解释了出生时观察到的所有性二态性泌尿生殖特征。约斯特的概念随后被扩展到包括大脑和行为的性别分化。虽然本综述的核心重点是泌尿生殖系统的发育，但我们假设本文中描述的新机制可能对大脑和行为的性别分化具有潜在的重大影响，这在该领域的历史上有先例。与约斯特理论的“特定”要求相反，雌性斑鬣狗和大象在性腺分化之前最初发育出雄性类型的外生殖器。此外，给怀孕的雌性斑鬣狗施用抗雄激素并不能阻止被治疗雌性后代形成阴囊、假阴囊、阴茎或阴茎状阴蒂，尽管目前尚不清楚雄性生殖器的形成是否涉及其他类固醇，或者是否存在绕过激素介导物的遗传机制。袋鼩在出生后在育儿袋中发生性别分化，为性别二态性的直接遗传控制提供了最确凿的证据，在性腺分化之前，阴囊仅在雄性中发育，育儿袋和乳腺仅在雌性中发育。雌性育儿袋和乳腺以及雄性阴囊的发育由X染色体上的基因控制。与约斯特理论的“扩展”版本一致，胎儿睾丸分泌的雄激素目前最能解释斑鬣狗生殖形态和内分泌学中广泛的性别差异，雄激素对袋鼩前列腺和阴茎的发育至关重要。但雄性袋鼩中关键的循环雄激素是5α雄甾二醇，在靶组织中局部转化为双氢睾酮，而在怀孕的雌性鬣狗中，母体卵巢分泌的雄烯二酮由胎盘转化为睾酮（和雌二醇）并转移到发育中的胎儿体内。睾丸睾酮似乎确实是雄性大象发情期行为现象背后的原因。斑鬣狗和大象都表现出母系社会组织，并且在这两个物种中，雌性生殖器形态需要雌性的配合才能成功交配。我们得出结论，在这些哺乳动物中，并非性别分化的所有方面都由睾丸激素决定。此外，我们建议对这些非传统物种泌尿生殖系统发育的研究将注意力引向可能在更常见的实验室哺乳动物的形态和行为性别分化过程中起作用的过程，尽管方式不那么显著。
