Urogenital System of the Spotted Hyena (Crocuta crocuta Erxleben): A Functional Histological Study Gerald R. Cunha, 1 * Yuzhuo Wang, 1 Ned J. Place, 2 Wenhui Liu, 3 Larry Baskin, 3 and Stephen E. Glickman 2 1 Department of Anatomy, University of California, San Francisco, California 94143 2 Department of Psychology, University of California, Berkeley, California 94720 3 Department of Urology, University of California, San Francisco, California 94143 ABSTRACT The unique urogenital anatomy and histol- ogy of female spotted hyenas (Crocuta crocuta Erxleben) was reexamined to identify adaptations of “structure” that enable/facilitate urination, mating, and parturition through the clitoris. Unusual features of penile anatomy required for meeting ceremonies and successful mating through a clitoral point of insertion were also examined. As reported previously, the upper urogenital tract of the female spotted hyena is typical of other carnivores and consists of the oviducts, uterine horns, uterine body, and vagina. An anatomically defined cervix is absent, even though a histologically defined transition zone between the uterine body and vagina was demonstrated. Adaptive features of the upper genital tract were a helical-shaped uterine cavity, extensive smooth muscle in the uterus and vagina, and a newly discovered submucosal mucous uro- genital gland (SMUG) located immediately caudal to the vagina. The extensive smooth muscle facilitates the expul- sion of the large pups at parturition through the recurved birth canal. Secretions of the SMUG provide lubrication and protection for the urogenital mucosa during mating and parturition. Two types of “erections” are suggested by behavioral observations: the common hemodynamic erec- tion required for insertion and thrusting by the male, and phallic “flipping” that commonly occurs earlier in the mat- ing sequence and is sometimes seen during meeting cere- monies. Phallic “flipping” appears to be accomplished by the coordinated contractions of the large ischiocavernosus and retractor muscles acting on the semirigid organ. The extremely thick tunica albuginea and interstitial collagen of the common corporal body of the penis and clitoris gives the flaccid phallus some degree of rigidity even in the resting state in males and nulliparous females. Phallic “flipping” implies a hinge region in which flexibility is the key feature. Such a proximal hinge region of the male and female phallus was defined and was notable for its dimin- ished collagen content. The urogenital sinus traversing the clitoris was specialized for distensibility, thus facili- tating receipt of the penis during mating and for passage of the infant to the tip of the glans clitoris, where it emerges at parturition. The morphology of the glans penis is notable for the tapered common corporal body that extends to the distal tip of the glans. This adaptation is suggested to be required for a clitoral (as opposed to a vaginal) point of insertion during mating. Finally, addi- tional segments of erectile tissue devoid of a thick collag- enous capsule were demonstrated in the glans penis and glans clitoris, which appear to account for the “partially- locking” of the male into the female during the late stages of a mating sequence. Taken together, it is evident that the unusual sexual behaviors of the male and female spotted hyenas are facilitated by unique structural modi- fications of the relevant organs. J. Morphol. 256:205–218, 2003. © 2003 Wiley-Liss, Inc. KEY WORDS: spotted hyena; female urogenital tract; male urogenital tract; clitoris; penis The unique urogenital anatomy of the female spotted hyena has drawn human attention for sev- eral thousand years to ideas about hermaphroditism and/or the ability of these animals to change sex from year to year, commonly expressed in Western writings well into the last century (Glickman, 1995). Female spotted hyenas (Crocuta crocuta) have no external vagina, as the labia have fused during fetal life to form a pseudo-scrotum (Fig. 1). The clitoris has developed until it is the approximate size and shape of the male penis and is traversed by a central urogenital canal, which serves as a common pas- sageway for urinary and reproductive functions. The clitoris also has erectile capabilities roughly equiv- alent to those of the male (Fig. 2). In considering the functional aspects of the urogenital anatomy of the female spotted hyena, three unique aspects of the system must be kept in mind: 1) the female spotted hyena receives the male during mating through the clitoral meatus and the clitoral portion of the urogenital canal (Fig. 3); 2) the female spotted Contract grant sponsor: NIH; Contract grant number: MH-39917. *Correspondence to: G.R. Cunha, Department of Anatomy, Univer- sity of California, 3rd and Parnassus, San Francisco, CA 94143. E-mail: grcunha@itsa.ucsf.edu DOI: 10.1002/jmor.10085 JOURNAL OF MORPHOLOGY 256:205–218 (2003) © 2003 WILEY-LISS, INC.