Undifferentiated stage of gonad formation

Although the origin of the somatic gonadal cells is unresolved, three cellular sources have been proposed: local mesenchymal cells, coelomic epithelium and cells derived from the mesonephric tubules. It is proposed that the principal cells contributing to the gonadal primordia migrate from the degenerating mesonephric tubules to the presumptive gonadal tissue. Some cells contributing to the gonadal primordia may be derived from the coelomic epithelium and also from the underlying mesenchyme. Following proliferation of the coelomic epithelium and underlying mesenchyme, gonadal primordia develop as bilateral ridges. These ridges, which develop medial to the mesonephros and project into the coelomic cavity where they become covered by coelomic epithelium, extend from the thoracic to the lumbar region. The outline appearance of the gonadal ridges precedes the arrival of the primordial germ cells in the area. The undifferentiated gonads consist of primordial germ cells and mesodermal cells. The invading mesonephric cells and the mesonephric tubules form a tubular network called the rete system which consists of extra‐gonadal cords, connecting cords and intra‐gonadal cords (Fig 21.2). During development, as a consequence of proliferation in its mid‐region, the developing gonadal ridge assumes a globular appearance and remains attached to the mesonephros by a fold of mesothelium. Because of their morphological similarity, it is not possible to distinguish male primordial gonads from female primordial gonads at an early stage of development using histological methods. However, using modern molecular techniques, the sex of an embryo can be reliably confirmed at an early stage of development.

Differentiation and maturation of the testes

In genotypic males, the mesonephric cells at the periphery of the intra‐gonadal rete system develop into cords into which primordial germ cells become incorporated. These cords, known as seminiferous cords, become horseshoe‐shaped and their extremities join with mesonephric cells at the centre of the developing gonad (Fig 21.3). The seminiferous cords become convoluted and form the tubuli contorti. During this period of development, the seminiferous cords are solid structures, approximately 40 μm in diameter. On cross‐section they are composed of a peripheral layer of 15 to 20 mesonephric cells which are destined to become Sertoli cells. These mesonephric cells surround a central core of up to four germ cells, the pre‐spermatogonia. Later, a layer of mesonephric‐derived myoid cells surrounds the cords. Under the influence of the seminiferous cords, mesodermal cells, located between the cords, differentiate into the interstitial cells (Leydig cells) of the testis, which produce testosterone. Subsequently, the mesonephric cells at the centre of the developing gonad give rise to the tubules of the rete testis. In cattle and dogs, interstitial cells increase in number until birth and then decrease. In horses, they undergo marked hypertrophy between days 110 and 220 of gestation and then decrease in number. The highest rate of secretion of testosterone is reached when the interstitial cells are most numerous.

Mesenchymal cells under the coelomic epithelium of the developing testis develop into a fibrous layer known as the tunica albuginea. The mesenchymal cells between adjacent tubuli contorti form connective tissue septa which divide the testis into a number of lobules, while mesenchymal cells surrounding the tubules of the rete testis form a fibrous network called the mediastinum testis. The extent to which the testicular septa and the mediastinum testis become organised varies in individual species. In pigs, dogs and cats, they are well developed but in ruminants they are less well developed. In horses, the testicular septa contain smooth muscle cells, and the rete testis, which is atypical in that it does not occupy an axial position, is confined to the cranial pole of the testis where it extends through the tunica albuginea. Through the secretion of an inhibitory factor, the Sertoli cells, which surround the pre‐spermatogonia, prevent further differentiation of the germ cells until, at puberty, the seminiferous cords become canalised and form tubules. Seminiferous tubules form and spermatogenesis begins in sheep at approximately five months of age, in cattle at around six to eight months, in dogs at approximately nine to ten months, in horses at about two years and in humans at 12 to 14 years.

Differentiation and maturation of the ovaries

Although the origin of the sex cords is contentious, in genotypic females it is probable that they derive from the mesothelial cells surrounding the gonads. The sex cords form irregular recognisable structures into which germ cells become incorporated (Fig 21.4). Following breakdown of the sex cords, germ cells undergo a period of enhanced mitotic activity in the developing ovaries. The germ cells are organised into nests, which contain numerous oogonia linked by cytoplasmic extensions. Irrespective of the duration of oogonial mitosis within a species, in the majority of mammals it ceases before or shortly after birth (Table 21.1). As individual oogonia complete their period of mitotic activity, the germ cell nests degenerate and the oogonia become surrounded by a layer of squamous somatic cells of mesothelial origin, termed follicular cells. A germ cell enclosed in a basal lamina and surrounded by follicular cells constitutes a primordial follicle. The follicular cells induce the enclosed oogonium to enter the prophase of meiosis I. At this stage the germ cells, which are referred to as primary oocytes, undergo a prolonged resting or dictyate stage. Although some maturation of primary oocytes may occur, these germ cells do not progress to the tertiary stage of development until stimulated by gonadotrophic hormones at the onset of puberty.

Following the advent of puberty, recurring cyclical stages of follicular maturation occur in response to gonadotrophic hormones. As folliculogenesis proceeds, the squamous follicular cells, which become cuboidal, form stratified layers and are referred to as granulosa cells. Female mammals have their full complement of primary oocytes before or shortly after birth. In the ovary, germ cell proliferation and follicular development are confined to the peripheral areas of the developing gonad. By the end of this developmental period in domestic species, with the exception of horses, the ovary consists of a dense outer cortex which contains the follicles and a less dense central medulla composed of degenerating intra‐gonadal tubules, the rete ovarii. In cattle, sheep and pigs, follicles are randomly distributed in the cortex while, in dogs and cats, they occur in clusters. In mammals, a high percentage of oogonia and primary oocytes undergo degenerative change referred to as atresia, during prenatal and postnatal life. Approximate numbers of germ cells in the ovaries of bovine embryos and foetuses are presented in Table 21.2. Data relating to the approximate numbers of germ cells in canine ovaries from birth to 10 years of age are presented in Table 21.3.

Features of equine gonadal development

Development of follicles in the equine ovary is concentrated in the central area corresponding to the medulla in other species, while the non‐follicular area is located peripherally. During in utero development, the unattached surface of the ovary becomes concave and, because it is from this site that ovulation occurs, the concavity is referred to as the ovulation fossa.

The equine foetal gonads exhibit remarkable growth from approximately day 110 to day 220 of gestation. This enlargement, which occurs in both the developing ovary and testis, is attributed to hyperplasia and hypertrophy of interstitial cells. It has been suggested that gonadal enlargement is due to the action of equine chorionic gonadotrophin produced by endometrial cup cells. However, as the rate of gonadal development is maximal at the time that gonadotrophin activity has declined, this explanation is questionable. An alternative suggestion is that the increased gonadal size is due to the high levels of oestrogens produced by the placenta. However, as gonadal size decreases before maximum oestrogen production is reached, this suggestion seems improbable.

A notable feature of the developing equine testes is the appearance of pigment cells in the interstitial tissue during the ninth month of gestation. Prior to this time, the foetal testes have a yellowish‐white appearance but thereafter they gradually acquire a dark appearance. Pigmentation, which persists until after birth, is considered to be associated with degeneration of interstitial cells.

Genital ducts

Irrespective of the genotype of the developing embryo, both male and female genital ducts form during the undifferentiated stages of gonadal formation. Differentiation of the male and female genital duct systems from the undifferentiated duct system is outlined in Figure 21.5. In the male embryo, elements of the mesonephric (Wolffian) duct system which persist are incorporated into the male genital system, while, apart from vestiges, the paramesonephric (Müllerian) ducts largely disappear. In the female embryo, paramesonephric ducts contribute to the formation of the genital duct system, while the mesonephric ducts atrophy except for vestiges. The paramesonephric ducts are located lateral to the mesonephric ducts.

Differentiation of the female duct system in mammals

The primordia of the paramesonephric ducts arise from intermediate mesoderm lateral to the cranial ends of the mesonephric ducts. Initially, grooves which form in the coelomic epithelium give rise to paramesonephric ducts which move deeper into the mesenchyme adjacent to the related mesonephric ducts (Fig 21.2). The cranial portions of the paramesonephric ducts form the uterine tubes, while the caudal portions of the ducts give rise to the uterine horns, uterine body and cervix. At their cranial aspects, the uterine tubes remain open and communicate with the coelomic cavity. Postnatally, this communication persists as the abdominal ostium. At first, the portions of the ducts which are closed elongate caudally, lateral to the mesonephric duct (Fig 21.5). Close to the urogenital sinus, each duct occupies a position ventral to the mesonephric duct and fuses in the midline with its corresponding duct from the opposite side. The closed end of the fused ducts continues to grow caudally and makes contact with the urogenital sinus where it induces cellular proliferation of the endoderm of the urogenital sinus and the formation of the vaginal plate. Differences observed in the final anatomical arrangement of uteri in different species can be attributed to the relative positions of their primordial structures and the extent to which fusion occurs. In rodents and rabbits, fusion is confined solely to the outer portions of the walls of the ducts while the lumina remain distinct. This results in a separate opening for each uterine lumen into the vagina (uterus duplex). In domestic species, the caudal ends of the ducts fuse. Subsequently, the medial fused walls atrophy resulting in the formation of a single tube, the body of the uterus, which has a single opening into the vagina. Those portions of the ducts cranial to the region of fusion remain distinct and are the primordia of the horns of the uterus and the uterine tubes. Thus, in domestic animals the uterus which consists of two horns and a body is referred to as a bicornuate uterus (Fig 21.6). In cattle, the primordia of the paramesonephric ducts appear at approximately the 34th day of gestation and fuse with the urogenital sinus at approximately the 50th day. In primates, including humans, extensive fusion of the paramesonephric ducts occurs with associated atrophy along the median line of fusion, resulting in the formation of a large uterine body termed a uterus simplex (Fig 21.6).

The vagina is derived from both the vaginal plate and the fused ends of the paramesonephric ducts. Subsequently, cannulation of these fused structures occurs forming the lumen of the vagina. Initially, the lumen of the vagina is separated from the urogenital sinus by a thin membrane, the hymen, which subsequently breaks down. In domestic animals, persistence of hymen remnants is less evident than in primates. The caudal portion of the urogenital sinus forms the vestibule (Fig 21.7).

Epithelial buds, which arise from the primitive urethra and definitive urogenital sinus, form the urethral and vestibular glands, the female homologues of the prostate and bulbourethral glands in the male embryo.

Apart from some remnants of the excretory tubules and a small portion of the mesonephric duct, the female mesonephric system atrophies. The cranial remnants of the mesonephric tubules form the epoophoron (Fig 21.5). The mesonephric tubules caudal to the developing gonad become the paroophoron and the remainder of the mesonephric duct usually degenerates. Occasionally, a caudal portion of the duct persists as Gartner’s duct, which may form a cyst in the vaginal wall.

Avian gonads and associated ducts

Two primordial gonads and duct systems develop in avian embryos. In genotypic male embryos, two gonads and two duct systems persist and become functional. In almost all genotypic female embryos, the left gonad and its associated duct continue to develop into functional structures, while the right gonad and associated duct remain rudimentary. The left paramesonephric duct gives rise to the different regions of the female reproductive tract from the ovary to the cloaca.

Formation of the genital fold

The urogenital system, which develops retroperitoneally, bulges into the peritoneal cavity. With the degeneration of the mesonephros, the gonads and genital ducts become suspended by thin folds of peritoneum. The caudal portions of the genital ducts meet and fuse in the midline. Fusion of their associated peritoneal folds forms the genital fold (Fig 21.8). In the female, this sheet of peritoneum is referred to as the broad ligament of the uterus and is composed of three segments, the mesovarium which suspends the ovaries, the mesosalpinx which suspends the uterine tubes and the mesometrium which suspends the uterus. In the male embryo, that part of the genital fold which suspends the testes is termed the mesorchium and the portion which suspends the ductus deferens, the mesoductus deferens.

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