Book - Comparative Embryology of the Vertebrates 4-18

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Nelsen OE. Comparative embryology of the vertebrates (1953) Mcgraw-Hill Book Company, New York.

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Part IV - Histogenesis and Morphogenesis of the Organ Systems

Part IV - Histogenesis and Morphogenesis of the Organ Systems: 12. Structure and Development of the Integumentary System | 13. Structure and Development of the Digestive System | 14. Development of the Respiratory-buoyancy System | 15. The Skeletal System | 16. The Muscular System | 17. The Circulatory System | 18. The Excretory and Reproductive System | 19. The Nervous System | 20. The Development of Coelomic Cavities | 21. The Developing Endocrine Glands and Their Possible Relation to Definitive Body Formation and the Differentiation of Sex

The Excretory and Reproductive Systems

A. Introduction

1. Developmental Relationships

The excretory and reproductive systems often are grouped together as the urogenital system. This inclusive term is applied to these two systems because they are associated anatomically in the adult form and, during development, show marked interrelationships and dependencies.

An important relationship, shared by the developing reproductive and excretory systems, involves the caudal end or cloaca of the developing digestive tube. It is this area of the differentiating metenteron which affords an outlet to the external environment for the urogenital ducts in the majority of the vertebrate species. This fact will become obvious later.

2. Functions of the Excretory and Reproductive Systems

The functions of the reproductive systems of the male and female are discussed in Chapters 1 to 4 and 22.

The excretory system is most important in the maintenance of life, and is an important feature in the flow of fluids through the body as described in the introduction to Chapter 17. Food substances and water pass into the body through the walls of the digestive tract, and oxygen is admitted through the respiratory surfaces. The veins convey these substances to the heart and arteries (with the exception of fishes and some amphibia where oxygen passes directly into the arterial system), and the heart and arteries propel them to the tissues. Flere the food substances and water are utilized, and excess


Fig. 344. Regions of kidney origin within the vertebrate group; types of renal units formed. (A) The regions in the body where the different types of vertebrate kidneys arise. The pronephric tubules and the pronephric duct are shown in black to emphasize the fact that this part of the developing renal system is a fundamental and necessary primordium without which later kidney development is distorted. (B) Differentiation of the anterior portion of the nephrotomic plate and the common method of origin of the pronephric duct. In the anterior region (toward the left in the figure) the nephrotomic plate segments into individual nephrotomes from each of which a renal tubule arises (see tubules 1 to 5). Tubules 6-9 is a vestigial area of tubule development. The anterior mesonephric region indicated by tubules 10 to 15, etc. In the anterior mesonephric area, e.g., tubules 10 and 11, the individual tubules show a tendency to arise segmentally, but in more posterior mesonephric regions, e.g., tubules 12 to 15, etc., the tubules arise through condensation of cellular masses within the nephrogenic cord. Hence, primitive

(Continued on facing page.)



salts, wastes, and water are the by-products. The veins, lymphatics, and arteries convey these substances to the areas of elimination as follows:

(1) Carbon dioxide and water are residues of carbohydrate metabolism. The carbon dioxide and some of the excess water in the body are discharged through the respiratory surfaces.

(2) The products of protein breakdown together with excess water and mineral salts are conveyed mainly to the kidneys and are eliminated there.

Exceptional areas exist for the elimination of some of the above-mentioned materials. For example, a certain amount of salts, nitrogenous wastes, and


Fig. 344 — (Continued)

segmentation is lost. The pronephric duct is formed through coalescence of the outer distal portions of the pronephric tubules (see tubules 3, 4, and 5). The coalesced portion thus formed grows caudally to join the cloaca. The mesonephric tubules, however, appropriate the pronephric duct in a secondary manner, growing outward to join this duct (see tubules 10 to 12). The pronephric duct, after this appropriation, becomes the mesonephric or Wolffian duct.

Figs. 344C-F are diagrams of different types of renal units (nephrons) which appear in developing vertebrate kidneys.

(C) This diagram represents a form of renal unit which we may designate as Type I. It is a vestigial tubule which may or may not become canalized. Its chief function is to initiate the formation of the pronephric duct. It is found in the pronephric kidneys of elasmobranch fishes, reptiles, birds, and mammals and, to some extent, in the anterior portion of the mesonephric kidneys of these groups.

(D) This diagram represents a renal unit found typically in the pronephric kidneys of larval forms such as that of the frog tadpole. It is designated as Type II. It possesses a ciliated nephrostome connecting with the coelomic cavity and a secretory portion which joins the pronephric duct.

(E) This diagram is given to represent the typical form of renal unit found in the earlier phases of mesonephric kidney development of lower vertebrates. It is called Type III. It is found also in the pronephric kidney of Hypogeophis (Gymnophiona) (see Brauer, ’02), With some modifications it may represent a type of renal unit found in the adult kidney of the urodele, Necturus maculosus (see fig. 345D).

(F) The Type IV renal unit is similar to Type III but lacks the ciliated nephrostomal connection with the coelomic cavity. It is the later renal unit of the mesonephric kidney of most fishes and amphibia and the typical renal unit found in the mesonephric kidney of reptile, bird, and mammalian embryos. With some elaboration it would represent the nephron (renal unit) found in the metanephric kidney of reptiles, birds, and mammals.

G.I., G.2., G.3., stages in development of the mesonephric tubule in the embryo of Squalus acanthias. G.l. and G.2. the tubule arises from the nephrotome in a segmental fashion and appropriates the pronephric duct. G.3. a later mesonephric tubule. In the latter tubule the nephrostomal connection with the coelomic cavity is lost. Observe that the tubule empties into the collecting duct, an outgrowth of the mesonephric duct. The early primitive segmental condition is lost and many tubules are formed in each body segment, water pass off through the sweat glands of mammals; water and possibly small quantities of salts and wastes find riddance through the tongue’s surface and oral cavity of dogs; and the salt-excretory glands in the gills of teleost fishes remove excess salt materials from the blood, together with small amounts of nitrogenous substances. On the whole, however, the kidneys function to eliminate most of the nitrogenous residues and excess water, together with salt ions of various kinds, particularly those of chloride, sulfate, sodium, and potassium. The dispatch of salt ions by the kidneys is all important in maintaining the correct salt balance in the blood stream.

3. Basic Embryonic Tissues Which Contribute to the Urogenital Structures

The basic, embryonic, cellular areas which contribute to the formation of the excretory and reproductive structures are as follows:

(1) the nephrotomic plate (intermcdiatc-ccll-mass mesoderm) (fig. 344A).

(2) the adjacent coelomic tissue, underlying the nephrotomic plate during its development,

(3) the entodermal lining and surrounding mesoderm at the caudal end of the digestive tube, and

(4) the ectoderm of the integumentary areas where the urogenital openings occur.

(5) primordial germ cells.

B. Development of the Excretory System

1. General Description

The excretory system is composed of the following:

( 1 ) a series of excretory units, known as nephric units or nephrons,

(2) the kidney, a structure in which the nephrons are grouped together,

(3) a series of collecting ducts from a particular region of the kidney, which join the nephric units on the one hand and a main excretory duct on the other, and

(4) the cloaca (or its derivative, the urinary bladder) and a passageway to the external surface of the body (figs. 345A, B, D; 348G, D).

a. Types of Kidneys Formed During Embryonic Development

The kidney in Greek is called nephros and in Latin, ren. The words nephric and renal are adjectives, pertaining to the kidney but differing etymologically. By adding a prefix to the word nephros, various types of kidneys are denoted as follows:

(1 ) Holonephros is a word that was introduced by Price (1896) and designates a kidney derived from the entire nephrotomic plate in which a single nephron (nephric unit) arises from each nephrotome. (The word nephrotome is applied to each segmented mass or bridge of mesoderm, developed within the nephrotomic plate, which connects the somite to the unsegmented lateral plate mesoderm or hypomere. See figure 344B.) The early development of the kidney tubules in the hagfish, Polistotrema (Bdellostoma) stouti (Price, 1896), and in the elasmobranch fish, Squaliis acanthias (Scammon, Tl), tends to simulate holonephric conditions.

(2) Pronephros, mesonephros, metanephros, and opisthonephros are terms for types of kidneys. Actually, during the development of all gnathostomous vertebrates, the nephrotomic plate on either side produces not one holonephros but instead three types of kidneys which are adapted to three different developmental and functional conditions. These kidneys develop antero-posteriorly in three general regions of the nephrotomic plate (fig. 344A). The most anteriorly developed kidney is called the pronephros; the kidney which develops from the midregion of the nephrotomic plate is the mesonephros; and that which arises from the caudal end of the nephrotomic material is the metanephros. Kerr (T9) attaches the name opisthonephros to the kidney which arises posterior to the pronephros in the late larvae of fishes and amphibia. The opisthonephric kidney takes its origin from the entire caudal portion of the nephrotomic plate. It therefore represents the nephrogenic tissue of the posterior part of the embryonic mesonephric kidney plus the nephrogenic material which enters into the formation of the metanephric kidney of reptiles, birds and mammals.

. b. Types of Nephrons or Renal Units Produced in Developing Vertebrate Embryos

Four main types of renal units are produced during kidney development in various vertebrate species. Consult figure 344C-F.

2. Functional Kidneys During Embryonic Development

During embryonic development, the following types of functional kidneys occur in the gnathostomous vertebrates.

a. Pronephros

The pronephric kidney is functional in all species producing free-living larval forms. In these larvae it operates not only to remove waste materials but is essential also in the removal of excess water, thus preventing edema (Howland, M6, ’21; Swingle, ’19). Free-living larvae are found in teleost, ganoid and lung-fishes, and in the amphibia.

b. Mesonephros

In all free-living larvae the pronephros is succeeded by the mesonephros during the larval period. The decline of the pronephros and the ascendancy of the mesonephros is well illustrated in figure 335B-E relative to the developing venous system in anuran larvae. The mesonephric kidney also functions in the embryos of elasmobranch fishes, reptiles, birds, and mammals. In the mammals its efficiency as a renal orggn appears to be correlated with the degree of intimacy existing between the extra-embryonic and maternal tissues in the placenta. When this relationship is intimate (fig. 373D) as in rats, mice, humans, etc., the mesonephric kidneys are less developed, and therefore probably less functional, than in species such as the pig. In the pig the placental relationship between embryonic and maternal tissue is not so close as in the species mentioned above (fig. 373B), and the mesonephric kidneys are very large and well developed.


c. Metanephros and Opisthonephros

As indicated on p. 773 the metanephros is the kidney of the adult form of reptiles, birds, and mammals, while the opisthonephros is the mature kidney in fishes and amphibians. As the definitive or adult form of the body is achieved in both of these groups, the mature form of the kidney assumes the renal responsibilities.


3. Development and Importance of the Pronephric Kidney


a. General Considerations


Observation and experimentation upon the developing urinary and genital systems of gnathostomous vertebrates suggest that the pronephric kidney, and particularly its duct, the pronephric duct, are most important in the later development of the excretory and reproductive systems (Gruenwald, ’37, ’39, ’41). The pronephric kidney therefore may be regarded as fulfilling two important functions in the gnathostomous vertebrates, namely:


( 1 ) It operates as an early renal organ in free-living larval species, and

(2) It is a necessary precursor in the development of the reproductive system and the later excretory system.


The pronephric kidney develops from the anterior portion of the nephrotomic plate at about the level of the developing heart and stomach region (fig. 3 44 A and B). This area of the nephrotomic plate becomes segmented into separate nephrotomes (fig. 344 A and B). During the differentiation of each nephrotome in the pronephric area, the connection between the nephrotome and the dermo-myotome disappears, and a small dorso-lateral outgrowth from the middle portion of the nephrotome occurs (fig. 344B, 1 and 2). This cylindrical outgrowth proceeds dorso-laterally toward the developing skin and then turns posteriad and grows caudally (fig. 344B, 3). In the next posterior nephrotome, it meets a similar rudimentary tubule with which it unites (fig. 344B, 3 and 4). The area of union formed by these combined tubules grows caudal ward to the next nephrotome to unite with its tubule (fig. 344B, 5), etc. As a result, the fused portions of the pronephric tubules give origin to the pronephric or segmental duct (fig. 344B).

The above method of origin of the pronephric duct has been described for elasmobranch fishes, reptiles, birds, and mammals. A different method of pronephric duct origin occurs in the amphibia and teleosts where the pronephric duct apparently arises by a longitudinal splitting of the nephrotomic plate (Field, 1891; Goodrich, ’30). The pronephric duct, once formed, continues to grow caudalward above the nephrotomic plate until it reaches the caudal end of the plate. In this area, the growing end of the pronephric duct turns ventrally and joins the cloaca (figs. 344A; 346F).

The entire pronephric portion of the nephrotomic plate is never realized in the formation of pronephric tubules. The number of tubules actually formed varies greatly and is confined generally to a limited number of nephrotomes in the middle or posterior pronephric are^

b. Shark, Squalus acanthias

In Squalus acanthias, a considerable nephrotomic area, overlying the caudal portion of the developing heart in segments 5-11, may produce suggestive indications of pronephric tubule formation. However, generally only three to five pronephric tubules are definitely formed. The distal ends of these tubules unite to form the pronephric or segmental duct and the latter grows caudalward to join the cloaca. The pronephric tubules are aberrant and soon disappear, but the pronephric duct remains and when joined by the mesonephric tubules it becomes known as the Wolffian or mesonephric duct (fig. 347A).

c. Frog

In the frog, Rana sylvatica, Field (1891) describes the origin of the pronephric kidney from a thickening and outgrowth of the somatopleuric layer of the nephrotomic plate in segments 2-4. Three tubules arise from this thickened area, one tubule in segment two, another in segment three, and a third in segment four.

A cross section of the developing second pronephric tubule at a time when the neural tube is wholly closed and a short while before hatching is shown in figure 346A. At about the time of hatching the second pronephric tubule is well advanced, as indicated in figure 346B, and the fully developed first pronephric tubule of an embryo (larva) of about 8 mm. is shown in figure 346C. The entire pronephric kidney of one side consisting of three tubules viewed from the ventral aspect at the 8 mm. stage is presented in figure 346E. The general plan of the pronephric kidney at the 18 mm. stage is pictured in figure 346F. Figure 346D lies in plane A-D of figure 346F.

Contrary to the manner of origin of the pronephric duct from the distal ends of the pronephric tubules in the embryo of Squalus acanthias, Field describes the origin of this duct in the frog from a thickening of the somatopleuric layer of the nephrotomic plate in segments 4-9. This somatopleuric thickening separates, becomes canalized, and grows caudally to join the dorsal area of the cloaca, a union which is accomplished at about the time of hatching (fig. 25 8F'). The pronephric tubules in their development unite with the cephalic end of this duct.

As the development of the pronephric kidney advances it is to be observed that one large glomus is formed, projecting into the restricted coelomic chamber or nephrocoel which is shut off partly from the common peritoneal cavity by the expanding lungs (fig. 346D). Each ciliated nephrostome opens into this nephrocoelic chamber (fig. 346F). {Note: Reference may be made to figure 335A-C which shows the well-developed renal portal system inserted into postcardinal vein in relation to the pronephric kidney. The postcardinal vein breaks up into a series of small capillaries which ramify among the coiling pronephric tubules (see figure 346C) to be gathered up again into the posterior cardinal vein as it opens into the common cardinal vein.)

d. Chick

The pronephric tubules of the pronephric kidney of the chick are rudimentary, occupying a region of the nephrotomic plate, from the fifth to the sixteenth somites. However, all of the tubules do not appear simultaneously.

The pronephros begins to form at about the stage of 12 to 13 pairs of somites (stage 11, Hamburger and Hamilton, ’51, or at about 40 to 45 hrs. of incubation), and small aberrant tubules are formed (fig. 345E) which grow caudally to give origin to the pronephric duct as indicated in figure 344A.


Fig. 345. Developing kidney tubules. (A & B) General structure of adult human kidney. (A) This diagram represents a single renal unit in relation to blood vessels, collecting duct and the minor calyx. Arrows denote direction of excretional flow. The position of A in drawing B is shown by the elongated oblong in B. (A is redrawn, somewhat modified, from Glendening, 1930, The Human Body, Knopf, Inc., N. Y.) (B)

Human kidney, part of wall removed, exposing pelvis and other general structures. (Redrawn from Maximow and Bloom, 1942, A Textbook of Histology, Saunders, Philadelphia, after Brauer.) (C) Including C-1 to C-6. Stages in the development of a mesonephric renal unit in the frog, Rana sylvatica (C to C-6 redrawn from Hall, 1904, Bull. Mus. Comp. Zool. at Harvard College, vol. 45). C represents a section through a developing mesonephric tubule showing cellular condensation in relation to pronephric (mesonephric) duct. C-1 to C-6 are diagrammatic figures of a developing renal unit from right side of body. The somatic or lateral portion of the tubule is shaded by lines, the splanchnic portion is unshaded. (D) Diagrammatic representation of a section through pelvic kidney of Necturus maculosus. (Redrawn and modified from Chase, 1923, J. Morph., 37.) A tubule of the ventral series is shown with a peritoneal canal and ciliated nephrostome which opens into the coelomic cavity. A tubule of the dorsal series also is depicted. The latter type of tubule lacks a ciliated nephrostome opening into the coelom. (E) Pronephric tubule in the chick. Section passes through somite 11 of embryo of 16 17 somites. (F) Section through mesonephric kidney of 96 hr. chick embryo, partly schematized. (G) Schematized section through mesonephric kidney of six to seven day chick.


At the 16- to 21 -somite stage, the pronephric kidney is well developed, but not all the tubules are present. At the 21 -somite stage, pronephric tubules are present from the eleventh to fifteenth somites. Anterior to this area, they are degenerate and rudimentary. At the 3 5 -somite stage (65 to 70 hrs. of incubation or stage 18, Hamburger and Hamilton, ’51 ), the pronephric kidney as a whole is undergoing degeneration, although the pronephric duct (now the mesonephric duct) remains and, at this time, joins the dorso-lateral area of the cloaca.


e. Mammal (Human)

In the human embryo, the pronephric rudiments extend from the seventh to the fourteenth somites (fig. 344A), although rudimentary conditions may extend as far forward as segment 2 (Felix, ’12). The pronephric kidney appears in embryos of about 9 to 10 pairs of somites, and begins to degenerate at a stage of 23 to 28 segments. As in the chick and the shark, the pronephric duct arises from the fusion of the dorso-lateral ends of the rudimentary pronephric tubules and grows caudalward to open into the ventro-lateral aspect of the cloaca in embryos of 4.2 mm., greatest length (fig. 344A). (See Felix, ’12.)

Although the human pronephros is vestigial, it is as well developed as in any other mammalia.

/ 4. Development of the Mesonephric Kidney

The mesonephric kidney develops in the region of the nephrotomic plate posterior to the pronephric kidney (fig. 344A). Five features distinguish the mesonephric kidney from the pronephric kidney:

(1) The primitive segmentation manifest in the origin of the pronephric kidney tubules is lacking generally in the mesonephric kidney, although there is a tendency for the tubules to arise segmentally in the anterior region. Also, a segmental origin of the tubules throughout the length of the early mesonephros occurs in the embryo of the hagfish, Pollstrotrema (Bdellostoma) stouti (Price, 1896), and a primitive segmental condition is found in the early mesonephros of the shark and frog embryos as indicated below.

(2) The mesonephric tubules join the previously formed pronephric duct and thus appropriate this duct. The pronephric duct then becomes the mesonephric (Wolffian) duct.

(3) The antero-posterior extent of the mesonephric kidney is much greater than the pronephric kidney, the mesonephric kidney utilizing the greater part of the nephrotomic plate.

(4) An innovation, the collecting duct system, is introduced in the mesonephric kidney as a result of outgrowths from the mesonephric duct.


Fig. 346. The developing pronephric kidney in the frog, Rana sylvatica (A-C and E, redrawn from Field, 1891, Bull. Mus. Comp. Zool. at Harvard College, vol. 21. E considerably modified). (A) Transverse section through developing second pronephric tubule of frog embryo at a time when the neural tube is completely closed, two gill fundaments are present and the otic vesicle is a shallow depression. (B) Same tubule at about the time of hatching. (C) Section through first pronephric tubule at 8 mm. stage. (D) Transverse section through second pronephric tubule, see line d, fig. 346F, of 18 mm. Rana pipiens tadpole. (E) Entire pronephric kidney of one side of 8 mm. R. sylvatica embryo. (F) Schematic reconstruction of 18 mm. R. pipiens tadpole looking down from dorsal area upon the pronephric kidneys and the developing mesonephric kidneys.


The renal units empty their products into these collecting ducts in the mature form of the kidney.

(5) Whereas the functional pronephric kidney is confined to those species which develop free-living larvae, the mesonephric kidney is functional in all vertebrate embryos with the possible exception of a few mammalian species?)

a. Squalus acanthias

The mesonephric tubules in the embryo of Squalus acanthias and in other elasmobranch fishes originate in a manner similar to the pronephric tubules. That is, a single tubule arises from each nephrotome of the nephrotomic plate. In doing so, the nephrotome loses its connection with the developing somite or dermo-myotome, and its dorso-lateral aspect thickens and grows laterad in the form of a tubule. This tubule comes in contact, and fuses, with the pronephric or segmental duct (fig. 344B, 11; G.l, G.2). The latter then becomes the mesonephric or Wolffian duct. In the 20.6-mm. embryo of Squalus acanthias according to Scammon (’ll), 37 pairs of these tubules are present, extending along the mesonephric duct to the cloaca (fig. 347A). Later, this primitive segmentation is lost, and many tubules are developed in each segment. The anterior portion of the kidney soon degenerates; the nephrostomal connections of the mesonephric tubules with the coelom established during the development of the tubules are lost; and the mesonephric tubules assume the general morphology shown in figure 344G.3). As shown in figure 344G.3, a series of collecting ducts eventually develops to connect the mesonephric tubules with the mesonephric duct. Renal units eventually arise in the nephrogenous tissue overlying the cloaca. This area corresponds to the metanephric region of higher vertebrates, and the mature kidney of Squalus acanthias thus becomes a combination of caudal, mesonephric, renal units, associated with metanephric units. The mature kidney thus is an opisthonephros. (See Kerr, ’19, also p. 773). In the adult kidney, segmentally arranged nephrostomes may be observed in a limited area along the medial side of the kidney, although they do not connect with the renal units.

b. Frog

The mesonephric renal units in the frog begin to arise at about the 10-mm. stage. As in the shark embryo, the early origin of the mesonephric renal units is segmental. An intermediate zone of the nephrotomic plate between the developing mesonephros and the pronephric kidney does not develop renal units. Coincident with this fact those units which arise more posteriorly in the nephrotomic plate are developed better than those which arise anteriorly.

The renal units arise as cellular condensations of mesodermal cells within the cellular mass of the nephrotomic plate (fig. 345C-1). These cellular condensations elongate, become canalized, and assume a union with the mesonephric duct as shown in figure 345C-1 to C-5. A nephrostomal connection with the coelomic cavity also appears, but the nephrostomal segment soon acquires a secondary connection with a renal vein (fig. 345C, 4-6). The veins thus come to drain the coelomic cavity directly. (In the water-abiding urodele, Nectiirus maculosus, the nephrostomal connection remains in contact with some of the renal units, even in the adult. See figure 345D.)

As the mesonephric kidney of the frog continues to develop, many new mesonephric renal units are added, and several units appear in each body segment. In consequence the primitive segmental arrangement of the renal units is lost, particularly in the caudal region of the nephrotomic plate where the kidney is developed most highly. Collecting ducts develop as evaginations of the mesonephric duct and the renal units discharge their contents into these collecting ducts.

Caudally situated nephrotomic material, comparable to the metanephric area of the kidney of higher vertebrates, is incorporated along with the mesonephric kidney as in the shark embryo. The adult form of the kidney, therefore, may be regarded as an opisthonephros, composed of mesonephric and metanephric renal units.


c. Chick

The mesonephros of the chick develops from the nephrotomic plate in the region between the somites 13 and 30. The nephrotomic plate in the chick embryo increases its substance rapidly through cell proliferation posterior to the area of pronephric-kidney origin. The original nephrotomic plate in this way becomes converted into an elongated mass or cord of cells called the nephrogenic cord. The mesonephric tubules arise as condensations within this cord of nephrogenous tissue. The renal unit emerges initially as a rounded mass of epithelial cells as in the frog. These epithelial masses elongate. They acquire a Malpighian body at one end, while the other end unites with the mesonephric duct. Some of the anterior tubules may have coelomic connections, similar to the pronephric tubules, but as this portion of the mesonephric kidney degenerates, these nephrostomal structures have little functional significance.

As development progresses, the nephrotomic substance increases greatly through proliferation of its constituent cells, and several renal units arise in each body segment (fig. 345F). To aid this process, the mesonephric duct forms collecting ducts which extend outward into the region of the developing renal units, and a group of these units joins each collecting duct (fig. 345G). The mature form of the mesonephric tubule of the chick consists of a glandular (secretory) segment which connects with either the mesonephric or the collecting duct on the one hand and with a Malpighian body and its glomerulus on the other (fig. 345G). The mesonephric kidney of the chick is a prominent ^^xcretory organ from the fifth to the eleventh day. During the developmental period from 8 to 10 days its tubular system is exceedingly complex compared to that shown in figure 345G. After this period, it begins to degenerate, and its function is taken over by the developing metanephric kidney.


d. Mammal

As in the chick, the mesonephric kidney in many mammalian embryos is a prominent excretory structure. However, in the rat, mouse, and certain other mammals its function as an excretory organ is dubious, probably resulting from the fact that the placental connection in these forms is sufficiently intimate to assume excretory functions. In the 10-mm. pig (figs. 261, 262), it is a prominent structure, filling a considerable part of the coelomic cavity on either side. In the human embryo, the condition is intermediate between that of the pig and rat. It possibly functions as an excretory structure in the human embryo.

The renal unit or mesonephric tubule which is evolved within the nephrogenic cord is similar to that of the bird. It develops from a condensed mass of epithelium within the nephrotomic plate (nephrogenic cord). This condensed, S-shaped mass elongates, becomes canalized, and joins the mesonephric duct. The mesial end of the tubule, in the meantime, develops a Malpighian body with its glomerules and vascular connections. The glandular tube is a highly coiled affair and is associated intimately with the veins as indicated in figure 344F. Collecting ducts, arising as evaginations of the mesonephric duct similar to those in the chick mesonephros, are formed.

("5. Development of the Metanephric Kidney

The metanephric kidney is the later embryonic and adult form of the renal organ in reptiles, birds, and mammals. As observed above, the mesonephric kidney involves three structures:

( 1 ) the urinary or Wolffian duct,

(2) a series of collecting ducts which evaginate from the mesonephric or Wolffian duct to connect with the renal units, and

(3) the nephrons or renal units.

These same relationships are present in the developing metanephric kidney.


Fig. 347. Urogenital system relationships in various vertebrates. (A) Reconstruction of 20.6 mm. embryo of Squalus acanthias. (Redrawn from Scammon, 1911, Chap. 12, Normentafeln Entwichlungsgeschichte der Wirbeltiere, by F. Keibel, G. Fischer, Jena.)

(B) Left side view of dissection of male pickerel, Esox Indus, showing reproductive and urinary ducts and absence of a cloaca. (Redrawn from Goodrich, 1930, Studies on the Structure and Development of Vertebrates, Macmillan and Co., Limited, London.)

(C) Male reproductive system, ventral aspect, of the pigeon. (Redrawn from Parker, lonfi Zootomy, Macmillan and Co., Limited, London, The Macmillan Co., N. Y.)

a. Chick

1) Metanephric Duct and Metanephrogenous Tissue. The metanephric kidney in the chick begins to arise at the end of the fourth day of incubation from a diverticulum which evaginates from the caudal end of the mesonephric duct as the latter enters the cloaca (fig. 259). The origin of the metanephric diverticulum is similar to that of the various collecting ducts of the mesonephric kidney, i.e., it arises a's an outpushing from the mesonephric duct. The metanephric diverticulum enlarges as its distal end grows forward and dorsad into the nephrogenous tissue of the caudal end of the nephrotomic plate in trunk segments 31-33. As the metanephric diverticulum enlarges and grows into the nephrogenous tissue in this area, the nephrogenous tissue separates from the mesonephric tissue and, together with the metanephric diverticulum, moves anteriad above the mesonephros to the anterior end of the mesonephros. During this process, the distal end of the metanephric diverticulum enlarges into the future pelvic cavity of the kidney. Numerous small secondary evaginations make their appearance and extend outward from this cavity. The secondary evaginations from the primary pelvic cavity of the kidney form the rudiments of the future collecting ducts of the kidney.

2) Formation of the Metanephric Renal Units. The formation of the metanephric renal units is similar to that of the mesonephric units. At about 7 to 8 days of incubation, the nephrogenous tissue around the terminal ends of the collecting-duct evaginations from the primary pelvic cavity of the kidney forms dense epithelial masses. Each of these masses of condensed nephrogenous tissue assumes an S shape. One end of the S-shaped rudiment unites with the distal end of the developing collecting duct, while the other end forms a Malpighian body or renal corpuscle. (Comparable stages involving the development of the S-shaped rudiment in the mammalian metanephric kidney are shown in figure 348 A-C.) By the eleventh day, well-formed renal units are found in the developing kidney.

The outer capsule of the kidney arises from the peripheral portions of the nephrogenous tissue and surrounding mesenchyme. The metanephric kidney is retroperitoneal in position, that is, it lies outside the peritoneal cavity proper.

The posterior end of the metanephric duct or ureter acquires an independent opening into the cloaca as the above changes occur, for the caudal end of the mesonephric duct is drawn into, merges with, and thus contributes to the cloacal wall as the cloaca enlarges.

b. Mammal (Human)

1) Formation of the Pelvis, Calyces, Collecting Ducts, and Nephric Units.

As in the bird, the metanephric kidney of the mammal has a dual origin. One part, the metanephric diverticulum, arises as an evagination from the caudal end of the mesonephric duct at the level of the twenty-eighth somite in the 5- to 6-mm. human embryo (fig. 348H). This evagination extends dorsally into the caudal end of the nephrotomic piate (nephrogenic cord). (See figure 348E.) The metanephric diverticulum enlarges at its distal end and thus forms the rudiment of the pelvis of the kidney as in the chick (fig. 348F). As the rudimentary pelvis enlarges, it sends out secondary evaginations, the rudiments of the future collecting ducts of the kidney (fig. 3481). Surrounding these secondary diverticula, there is the cellular substance (fig. 3481) of the metanephrogenous tissue, derived from the nephrogenic cord posterior to the caudal limits of the mesonephric kidney.


Fig. 348. The developing metanephric kidney. (A) Condensation of rudiment of renal tubule in relation to rudiment of arched collecting tubule. (B) Renal tubular rudiment has united with arched collecting tubule. (C) Later stage in differentiation of renal unit. (D) Final stage in development of renal unit. (E) Developing mesonephric and metanephric kidney of human embryo of about 5 weeks. (F & G) Mesonephric and metanephric conditions in human embryo of 8 mm. or about sixth week of development. (H) Diagram showing origin of metanephric uteric bud from caudal end of mesonephric duct in human embryo approximating 5.3 mm. greatest length. (Redrawn from Felix, 1912, in Chap. 19, Human Embryology, by F. Keibel and F. P. Mall, Lippincott, Philadelphia.) (I) Differentiation of kidney pelvis in human embryo of 20 mm. length or about seven weeks of gestation.


In human embryos of 14 to 15 mm. (about seven weeks), four definite primordia of the metanephric urinary system are established as follows (fig. 3481):

( 1 ) Nephrogenous tissue is present which surrounds beginning diverticula of the collecting ducts;

(2) a system of developing collecting ducts which represents evaginations from the primitive pelvis of the kidney;

(3) from the primitive pelvis of the kidney arise the rudiments of the anterior and posterior major calyces; and

(4) the primitive ureter (metanephric duct) of which the primitive pelvis is the distal enlargement.

(The word calyx refers to a rounded, distal division of the pelvis of the kidney. The plural form of calyx is calyces.)

From each major calyx, secondary or minor calyces arise (fig. 3481), and from each minor calyx, the primary or straight collecting ducts emerge into the surrounding, nephrogenous, cellular mass. Each primary calyx and its straight collecting-duct rudiments, together with the surrounding nephrogenous cells, form the rudiment of the future renal lobe.

The straight collecting ducts continue to elongate and push out into the surrounding nephrogenous tissue. In doing so, the distal end of each collecting duct sends out several (usually three or four) smaller evaginations into the surrounding nephrogenous material. These smaller terminal evaginations represent the rudiments of the arched collecting tubules of the collecting duct system (fig. 348A). Around each of the arched-tubule rudiments, masses of nephrogenous tissue condense into the S-shaped structure typical of the developing renal units of the mesonephric kidney of the frog, chick, and mammal and in the metanephric kidney of the chick. A sigmoid-shaped concentration of nephrogenous cells fuses with each arched collecting tubule and elongates distally, differentiating into the parts of the typical, mammalian, metanephric tubule (fig. 348A--D).

As the kidney continues to develop, the original primary or straight collecting ducts branch repeatedly, forming about 12 generations by the fifth month of human fetal existence. As these branches arise, the pelvis of the kidney and the calyces enlarge considerably, and some of the collecting ducts are drawn into and are taken up into the walls of the expanding calyces. In the fully formed kidney, about 20 of these large straight collecting ducts open into the papillary ducts at the apex of the renal lobe or pyramid into a minor calyx (fig. 3 45 A, B) (Felix. ’12). The outer peripheral portion of the kidney, containing the glomeruli and various parts of the renal units (nephrons), forms the cortex of the kidney, while the inner portion, in which lie the straight collecting and papillary ducts, forms the medulla (fig. 345B).

2) Formation of the Capsule. The metanephrogenous tissue around the developing pelvis and collecting ducts of the kidney becomes divided into inner and outer zones. The inner zone cells differentiate into the renal units, whereas the outer zone cells form the interstitial connective tissue and outer, connective-tissue capsule of the kidney.

3) Changes in Position of the Developing Kidney. The early developing kidney is located in the pelvic area at the caudal end of the mesonephric kidney. As the mesonephric kidney declines in size and moves caudally, the metanephric kidney pushes anteriorly and takes its final retroperitoneal position at birth in the region of the first lumbar area. (Cf. figs. 3B-F; 348E-G.)

6. Urinary Ducts and Urinary Bladders a. Types of Urinary Ducts

The following two types of urinary ducts were mentioned above:

(1) The pronephric duct, which later becomes the mesonephric duct, is the functional urinary duct in the larval embryonic form of fishes, amphibia, reptiles, birds, and mammals. It continues to be the main urinary duct in adult fishes and amphibia, particularly in the female. (See (2) below.)

(2) A second type of urinary duct represents an outgrowth of the mesonephric duct. Examples of this type are: (a) the metanephric duct and its branches in the kidneys of reptiles, birds, and mammals, (b) the collecting ducts in the mesonephric kidney of all vertebrates, and (c) the adult urinary ducts in the posterior kidney region of certain male fishes, such as are present in the shark, Squalus acanthias, and in the salamander, Triton taeniatus.

b. Urinary Bladders

During the development of the urinary system in the mammal, the ventral portion of the cloacal area and its allantoic diverticulum become separated from the dorsal cloacal or rectal area by the caudal growth of a fold of tissue, known as the urorectal fold or cloacal septum. The cloacal septum eventually divides the cloaca into a ventral bladder and urogenital sinus region, and a dorsal primitive rectum (fig. 348E--G). As this development proceeds, the proximal portions of the mesonephric and metanephric ducts are taken up into the wall of the caudal bladder region, and a considerable amount of mesoderm is contributed to the entodermal lining of the developing bladder. This mesodermal area presumably forms a part of the lining tissue of the bladder (fig. 349A, B). The metanephric duct or ureter, in the meantime, shifts its position anteriad and becomes united with the dorso-posterior portion of the bladder, while the point of entrance of the mesonephric duct migrates posteriad to empty into the anterior end of the dorsal region of the urogenital sinus (figs. 348F, G; 349A, B).

In turtles and in some lizards, the adult relationships of the urinary bladder and rectum are established in a somewhat similar manner to that of the mammals, although the caudal migration of the cloacal septum is not extensive. Also, the cloaca is retained.

The urinary bladder (or bladders) of some teleost and ganoid fishes arise as swellings and evaginations of the caudal ends of the mesonephric ducts (fig. 347B). A distinct urinary bladder is absent in elasmobranch fishes and in birds, but is present in amphibia as a ventral diverticulum of the cloaca.

c. Cloaca

A cloaca into which open the urogenital ducts and the intestine is a common basic condition of the vertebrate embryo. It is retained in the definitive or adult body form of elasmobranch fishes and to a considerable extent in dipnoan fishes. It is present also in the adults of amphibia, reptiles, birds (fig. 347C), and prototherian mammals. A cloaca is dispensed with in the adult stage of teleost (fig. 347B) and ganoid fishes, and also in the adult stage of higher mammals (fig. 349A-D).

C. Development of the Reproductive System

The general features of the adult condition of the reproductive system are described in Chapters 1 and 2. For most vertebrates, the reproductive system consists of the reproductive glands, the ovaries or testes, and the genital ducts.


Fig. 349. Differentiation of the caudal urogenital structures in the human embryo. (A) Later stage in differentiation of the cloaca; the rectal area is being separated from the ventrally placed urogenital sinus by the cloacal (urorectal) membrane. Condition of sixth week (about 12 mm.) embryo. (B) Rectal and urogenital areas completely separated. Mullerian and mesonephric ducts present. Metanephric duct has moved forward into the posterodorsal area of the developing bladder. The MUIlerian ducts have fused at their caudal ends to form the uterovaginal rudiment. This condition is present at about 8 weeks. (C) Male fetus of about 5 months. Testis beginning to pass into developing scrotal sac. (See also fig. 3.) (D) Female fetus of about 5 months.

(E to K) Stages in development of external genitalia. (E) Indifferent condition (about 7 weeks). (F) Male about tenth week. (G) Male about 3 months. (H) Male close of fetal life. (I) Female about tenth week. (J) Female about 3 months. (K) Female close of fetal life. (L & M) Stages in development of the broad ligament and separation of the recto-uterine pouch above from the vesico-uterine pouch below.


Fig. 349. (See facing page for legend.) S


Fig. 350. Sex gland differentiation. (A) Transverse section through early genital rudiment on medial aspect of mesonephric kidney in the 10 mm. pig embryo. (B) Transverse section through early sex gland of the chick about middle of sixth day of incubation showing ingression of sex cord of first proliferation. Observe primordial germ cells in germinal epithelium. Compare with fig. 345G. (Redrawn from Swift, 1915, Am. J. Anat., 18.) (C) Transverse .section through sex gland rudiment of human embryo

11 mm. greatest length. (Redrawn and slightly modified from Felix, 1912, Chap. 19, in Human Embryology, vol. II, by F. Keibel and F. P. Mall, Lippincott, Philadelphia.) (D) Transverse section through testis of human embryo 70 mm. head-foot length. (Redrawn from Felix, 1912. For reference see C above.) (E) Section through human testis of embryo 70 mm. head-foot length, showing connection between te.sticular cords (developing .seminiferous tubules) and developing rete tubules. (Redrawn from Felix, 1912, reference same as in C, above.) (F) Transverse section through testis of seventh month human embryo showing developing seminiferous tubules. (Redrawn from Felix,

{Continued on facing page.)


1. Early Developmental Features; the Indifferent Gonad

The gonads or reproductive glands are associated intimately with the developing mesonephric kidneys. The typical site of origin is the area between the dorsal mesentery and the anterior portion of the mesonephric kidney (figs. 345F, G; 350C). As development progresses, it tends to move laterad and in doing so becomes located along the mesial aspect of the developing mesonephric ridge (figs. 3A; 345G).

The reproductive gland arises as an elongated fold, the genital ridge or genital fold. The extent of this fold, in general, is longer than the actual site from which the rudimentary gonad or reproductive gland arises, and it may extend for a considerable distance along the mesonephric kidney. Felix (’06) designates three general areas of the primitive genital ridge:

(1) a gonal portion, from which the sex gland arises,

(2) a progonal area in front of the gonal area, which gives origin to the anterior suspensory ligament of the gonad, and

(3) an epigonal area behind, which continues caudally as a peritoneal support along the mesonephric kidney (fig. 3A).

The rudimentary structural parts of the early genital ridge in the gonal area, viewed in transverse section, consist of the following (fig. 350A-C):

(1) primitive germ cells (origin of the germ cells discussed in Chapter 3, sec figure 60),

(2) the germinal (coelomic) epithelium and the primitive sex cords and cells proliferated therefrom, and

(3) contributions from mesonephric tissue, forming in most vertebrates the rete tissue of the urogenital union together with the primitive mesenchyme of the gonad.

The first stages in the development of the gonad consist of a thickening of the germinal (coelomic) epithelium and of a rapid and copious proliferation of cells from its inner surface. The primitive (primordial) germ cells become associated with the thickened germinal epithelium and its proliferated cells, and migrate inward into the substance of the gonad with the cells of the germinal epithelium (fig. 350B).

As a result of the activities of the germinal epithelium, a mass of cells, the


Fig. 350 — (Continued)

1912, reference same as in C, above.) (G) Differentiating testis in the wood frog, Rana sylvatica. (Redrawn from Witschi, 1931, Sex and Internal Secretions, edited by Allen et al., Williams and Wilkins, Baltimore.) (H) Ingrowth of sex cords from germinal epithelium of ovary of 6 weeks old rabbit. (Redrawn from Brambell, 1930, The Development of Sex in Vertebrates, Macmillan, N. Y.) (I) Section through differentiating

ovary in the opossum, 63 mm. pouch young. (J) Differentiating ovary in the wood frog, Rana sylvatica. (Redrawn from Witschi, 1931, reference same as G, above.)


so-called epithelial nucleus (Felix, ’12), is deposited in the genital ridge between the coelomic (germinal) epithelium and the Malpighian (renal) corpuscles of the mesonephric kidney (fig. 350C). As the epithelial nucleus increases in quantity, the genital ridge bulges outward from the general surface of the mesonephric kidney, and, at the same time, the nuclear cells push into the mesonephric substance against the renal corpuscles (figs. 345G; 350A-C).

During the early stages of the proliferative activities of the germinal epithelium in most vertebrates, cellular cords, the sex or medullary cords, appear to arise from the germinal epithelium (fig. 350B). These cords of cells are composed as indicated above of epithelial and germ cells. However, in the mouse and in the human, the proliferative activity of the germinal epithelium is such that the cellular nucleus of the genital ridge arises without a visible, dramatic ingrowth of cellular cords from the germinal epithelium (Brambell, ’27; Felix, ’12). Still, the cellular sex cords or elongated masses of cells do appear as secondary developments somewhat later in the genital ridges of the mouse and human (fig. 350C).

The early gonad up to this stage of development represents an indifferent, bipotential condition, having the structural basis for differentiation either into the testis or ovary (see figs. 350C; 351C-3). The indifferent condition in the human sex gland is present when the embryo is about 11 to 14 mm. long, i.e., at about the sixth or seventh week; in the chick, it occurs during the sixth day of incubation; and in the frog, it is present during the larval period.

2. Development of the Testis a. Mammal (Human)

As the indifferent gonad begins to differentiate into the testis, the following behavior is evident:

( 1 ) The germinal epithelium becomes a distinct flattened membrane, separated from the primitive tunica albuginea. Unlike the conditions in the developing ovary, the germinal epithelium quickly loses its germinative character and forms the relatively inactive, superficial membrane of the sex gland (fig. 350D). (The tunica albuginea eventually becomes a connective tissue layer below the coelomic (germinal) epithelium of the male and female sex glands.)

(2) The primitive sex or medullary cords of the indifferent gonad grow more pronounced, and they possibly may segregate lengthwise into separate, elongated cellular masses (fig. 350D).

(3) These elongated cellular masses or primitive seminiferous tubules become remodeled directly into the later seminiferous tubules. In doing so, their distal ends (i.e., the ends toward the primitive tunica albuginea of the sex gland) appear twisted and show anastomoses with neighboring seminiferous tubules, while their proximal ends assume a straightened condition and project inward toward the area connecting the sex gland with the mesonephric kidney (fig. 350D).

(4) In the area between the inner ends of the developing seminiferous tubules and the Malpighian corpuscles of the mesonephric tubules, a condensation of cellular material occurs which forms the rete primordium (fig. 350D). From the rete primordium the future rete tubules are developed.

(5) As the rete tubules form, they unite with the inner straightened portions of the seminiferous tubules (the developing tubuli recti) and distally with the renal corpuscles (Malpighian bodies) of the mesonephric tubules (fig. 350E). The appropriated mesonephric tubules form to a considerable degree the efferent ductules of the epididymis.

(6) While the foregoing processes ensue, the sex gland gradually becomes separated as a body distinct from the mesonephric kidney and appears suspended from the kidney by a special peritoneal support, the mesorchium. Within the mesorchium are found blood vessels, lymphatics, and the efferent ductules of epididymis (fig. 350D).

(7) Coincident with these changes, mesenchyme between the developing seminiferous tubules forms a coating of connective tissue around each tubule. This connective tissue membrane gives origin to the basement membrane of the seminiferous tubule. Within the tubules, epithelial elements, primitive germ cells, and sustentacular elements (Chap. 3) or Sertoli cells appear. The Sertoli cells extend from the connectivetissue wall of the tubule inward between the epithelial and genitaloid cells. The genital cells lie close to the surrounding connective-tissue or basement membrane (figs. 8; 350F).

(8) Between the developing seminiferous tubules, the various cells, blood vessels, etc., of the interstitial tissue begin to appear (fig. 3 5 OF; see Chap. 1).

(9) Accompanying the foregoing transformations, the primitive tunica albuginea, which originally appeared as a narrow area, containing a few scattered cells between the germinal epithelium and the sex cords, becomes thickened and develops into a tough, connective-tissue layer, surrounding the testicular structures and separating the latter from the covering coelomic epithelium. This appearance of the tunica albuginea is one of the characteristic features of testicular development. Extending from the tunica albuginea inward between small groups of seminiferous tubules as far as the rete area or mediastinum, connectivetissue partitions are formed. These partitions are the septula. Each septulum comes to surround a small group of seminiferous tubules and thus divides the testis into compartments or lobules (fig. 7). Within each lobule, several seminiferous tubules are found, with the tubuli contorti or twisted portion of the tubules lying distally within the compartment and the tubuli recti lying proximally toward the rete testis and mediastinum.

The formation of the rete-testis canals and of the urogenital union in general has been the subject of much controversy. In the elasmobranch fishes, Brachet (’21) considered the rete-testis canals to be formed by the nephrostomial canals of the anterior mesonephric tubules which unite with the developing seminiferous tubules. In the frog, Witschi (’21) believed a condensation of cells in the hilus of the testis formed the rudiments of the rete tubules and that these rudiments unite with the mediastinal ends of the seminiferous tubules on the one hand and with the renal corpuscles of the mesonephric tubules on the other, forming the urogenital union. In the chick, it is possible that the rete tubules arise as outgrowths from the renal corpuscles (Lillie, ’30, p. 394). In the human, Felix (’12) concluded that the rete tubules arise from a rete rudiment in the testicular hilus, but de Winiwarter (’10) considered them as outgrowths from the renal (Malpighian) corpuscles of the mesonephric tubules.

b. Chick

The development of the testis in the chick closely resembles that described above for the mammal. The sex or medullary cords arise during the fifth and sixth days of incubation from the germinal epithelium (fig. 350B). For a detailed description, consult Swift, ’16, and Lillie, ’30.

c. Frog

The main essentials of testicular development in the frog follow the pattern described above. However, because the gonadal rudiment of the frog differs slightly from that described for the mammal, certain features are presented here.

The germinal epithelium of the primitive gonad of the anuran is thin, and the primitive germ cells lie, together with various epithelial elements, below the germinal epithelium. In the center of this primitive gonad is the slit-like primitive gonadal cavity. This cavity is surrounded by the germ cells, epithelial cells and germinal epithelium. This condition may be regarded as the indifferent stage of gonadal development.

In the differentiation of the testis, cellular strands, the rudiments of the future rete tubules, grow down into the primitive gonadal cavity from the mesonephric kidney. In the male, these mesonephric strands are thick and grow rapidly. The primitive germ cells and epithelial cells eventually grow inward across the primitive gonadal cavity and become clustered about the mesonephric strands (fig. 350G).

At first the germ cells and epithelial elements form cellular nests associated with the mesonephric strands. Later, the cellular nests and associated cells from the mesonephric strands elongate into the primitive seminiferous tubules.

These seminiferous tubules develop lumina and unite directly with the rete tubules which arise, in the meantime, from cells of the mesonephric strands. The distal ends of the rete tubules join with the Malpighian corpuscles of certain mesonephric tubules. The mesonephric tubules thus united to the rete tubules are, of course, joined to the mesonephric duct. In consequence, these mesonephric tubules become the efferent ductules or vasa efferentia of the testis (Witschi, ’21, ’29).

3. Development of the Ovary a. Mammal

1) Formation of Primary Cortex and Medulla. The early phases of differentiation of the ovary varies in different mammalian species. Two features, however, are constant — features that serve to distinguish the differentiating ovary from the testis. One of these features consists of the fact that the ovary is more retarded in its development than the testis; the testicular features appear sooner in the male embryo than do ovarian features in the female embryo. This is a negative difference, but nevertheless, it serves to distinguish the two sexes. Another constant and positive feature, however, is that the germinal epithelium in the ovary retains its proliferative activity, while, in the differentiating testis, this activity is lost in the early stages of differentiation.

In the cat and rabbit (de Winiwarter, ’00, ’09 ), and in the calf and opossum, the first stage of ovarian differentiation is indicated by a second proliferation of sex cords (Pfluger’s cords) from the germinal epithelium (fig. 350H and I). The earlier sex or medullary cords thus are pushed inward toward the hilus of the* ovary, and a definite compact primary cortex is established, containing cords of epithelial and germ cells. The medullary cords become broken up in the meantime and are pressed inward in the direction of the forming primary medulla of the ovary. Some of the germ cells of the medullary cords undergo the earlier stages of meiosis but soon degenerate.

Synchronized with the foregoing changes in the peripheral area of the ovary are transformations within the hilar region, that is, the area of the ovary nearest to the mesonephric kidney. A conspicuous feature of these changes is the ingrowth of mesenchyme and differentiating connective tissue from the mesonephric kidney. Three morphogenetic phenomena accompany this ingrowth :

( 1 ) Blood vessels grow into the ovary from the mesonephric kidney to form a primitive vascular plexus within the developing medulla.

(2) A concentration of mesenchymal cells appears in the area between the developing ovary and the mesonephric kidney. This concentration of mesenchyme is the rete blastema, or the rudiment of the rete ovarii.

(3 ) From the region of the rete blastema radiating columns of mesenchyme and differentiating connective tissue fibers extend outward through the medullary zone into the cortical zone of the ovary. These columns establish the septa ovarii. The septa ovarii branch distally, dividing the cortical zone into columns and compartmental areas of germ and epithelial cells.

The proliferation of sex cords (Pfluger’s cords) may continue from the germinal epithelium for an extensive period in certain mammals, such as the cat. De Winiwarter and Sainmont (’09) noted three successive periods, although Kingsbury (’38) was unable to find a clear-cut distinction between the first and second proliferation. In the developing opossum, active proliferation from the germinal epithelium may be observed up to a time just previous to the fourth month, following birth (Nelsen and Swain, ’42).

At an early stage of development, the primitive ovary in transverse section presents the following features (fig. 3501):

( 1 ) an outer proliferating germinal epithelium;

(2) a primitive tunica albuginea beneath the germinal epithelium, composed of epithelial and germ cells together with some connective tissue elements contributed by the ovarian septa;

(3) the primitive cortex, a compact layer within the primitive tunica albuginea, composed of masses of germ cells, egg cords, and epithelial elements, together with strands of differentiating mesenchymal cells. The mesenchymal strands from the ovarian septa segregate the egg cords into separate areas of germ cells and epithelial elements;

(4) internally, near the mesovarium or the peritoneal support of the ovary, is the primitive medulla composed of epithelial cells, mesenchyme, blood vessels, and some oocytes and oogonia;

(5) in the region of the mesovarium is a compact cellular mass, the rudiment of the rete ovarii, the homologue of the rudiment of rete testis in the male. The fundament of the rete ovarii continues rudimentary, but a framework of connective tissue is established in this area of the ovary similar to that of the mediastium in the testis, and

(6) from the area of the rete ovarii, radiating strands of mesenchymal cells, extend peripherally through the medulla and into the cortex, and thus establish the septa ovarii, i.e., septa of the ovary. Certain relatively large “interstitial cells” appear in the septula areas.

2) Formation of the secondary cortex and medulla. During later stages in ovarian development the following changes are effected:

( 1 ) The primitive tunica albuginea becomes converted into a relatively thick secondary tunica albuginea lying between the germinal epithelium and the cells of the cortical zone. It contains connective-tissue fibrils and fibers of larger dimension, together with mesenchyme and connective tissue cells. The changes in the developing tunica albuginea are associated with an ingrowth of cells from the ovarian septa into the albuginean tunic.

(2) The primitive cortex transforms into a thick secondary cortex, containing many oocytes, some of which are surrounded by epithelial cells. The complex of an oocyte enclosed by epithelial cells forms a primitive egg follicle, which in mammals is called a primary Graafian follicle. The complete development of the Graafian follicle, however, does not occur until sexual maturity, although earlier stages may be produced previous to this period.

(3) A secondary medulla is formed containing a connective tissue network, enclosing blood vessels. From these blood vessels branches extend into the cortex. Some genitaloid cells may be found in the medulla.

(4) The rete blastema remains as a compact mass of cells, sharply delimited from surrounding cells. It comes to lie in the area between the ovary and the mesovarium, and forms the rete ovarii.

The development of the human ovary differs somewhat from the account given above in that active proliferation of cortical cords from the germinal epithelium is problematical. The proliferation of cells in the developing human ovary appears more gradual, and the egg cords of the primary cortex are developed in a gradual manner from cells lying below the germinal epithelium of the undifferentiated gonad (Felix, T2, p. 904).

b. Chick

The pattern of ovarian development in the chick follows that of the mammal, and a cortex and a medulla are established. One clear distinction in the ovarian development in the chick compared with that in the mammal occurs, however, for the right sex-gland rudiment remains vestigial in the chick while the left rudiment develops rapidly into the ovary. Thus it is, that sex differences can be distinguished in developing chicks by macroscopic examination of the sex glands during the latter part of the second week of incubation. The enlarged appearance of the left ovary in the female chick becomes noticeable at this time.


c. Frofi

The developing ovary in the frog differs primarily from the developing testis in two ways:

( 1 ) The germ cells and accompanying epithelial cells remain peripherally near the germinal epithelium, where they multiply and increase in number; some of them enlarge during the formative stages of the oocyte.

(2) The mesonephric rete cords, which in the testis are much thickened, appear slender in the developing ovary and fuse to form the lining


Fig. 351. Development of the reproductive and urinary ducts in vertebrates. (A-1 to A-4) Development of the reproductive ducts in Squalus acanthias. In A-2 the origin of the ostial funnel or coelomic opening of the oviduct is presented as a derivative of the opening of one or more pronephric tubules into the coelomic cavity. In fig. A-3, the urinary or opisthonephric duct is independent of the mesonephric (pronephric) duct which now is the vas deferens. The opisthonephric duct appears to take its origin as an evagination from the caudal end of the original pronephric duct. (B-1 to B-4) Development of the reproductive ducts in the frog. B-1 is adapted from data given by Hall, 1904, Bull. Mus. Comp. Zool. at Harvard College, vol. 45. (C-1 to C-7) Development

of the reproductive and urinary ducts in mammals. The MUllerian duct arises as an invagination of the coelomic epithelium at the anterior end of the mesonephric kidney. (See fig. 35 ID.) Once its formation is initiated, it grows caudalward along the pronephric

(Continued on facing page.)


tissue of the ovarian sac or enlarged space within the ovary (fig. 350J) . The ovary of the fully developed frog (and amphibian ovaries in general) is saccular (Chap. 2).

4. Development of the Reproductive Ducts

Most vertebrate embryos, with the exception of those of teleost and certain other fishes, develop two sets of ducts, one set of which later functions as reproductive ducts. These ducts are the mesonephric, Wolffian or male ducts and the Mullerian or female ducts. In the elasmobranch fishes, the Mullerian duct arises by a longitudinal division of the mesonephric duct (fig. 351 A). In the Amphibia, the Mullerian duct takes its origin independently. Anteriorly it arises as a peritoneal invagination of the coelomic epithelium, in the region of the cephalic end of the mesonephros. Posteriorly, this peritoneal invagination, as it grows caudally, appears to receive, in some urodeles, contributions from the mesonephric duct (fig. 35 IB). In the Amniota the Mullerian duct arises independently by a tubular invagination of the coelomic epithelium at the anterior end of the mesonephric kidney (fig.


Fig. 351 — (Continued)

(mesonephric) duct to join the cloaca (see fig. 351, C-2). The metanephric duct or ureter arises as an evagination of the caudal end of the pronephric (mesonephric) duct (see fig. 344A). C-2 is a drawing of the urogenital system of a 26 mm. pig embryo

viewed from the ventral aspect. Note extent of Mullerian duct growth caudalward. C-3 represents a generalized indifferent condition of the urogenital system of the mammal. C-4 and C-5 are diagrams of later stages in the development of the female (C-4) and the male (C-5), These conditions pertain particularly to human embryos. However, by a division of the uterus simplex into a bicornate or duplex condition it may be applied readily to other mammals. (C-6) Later arrangement of reproductive ducts and the associated ovaries in the human female after the descent of the ovaries. Observe origin of various ligaments. (In this connection see also fig. 3.) (C-7) Later development of

the reproductive duct-testis complex in the human male, during descent of the testis into the scrotum. Observe origin of testicular ligaments. (See also fig. 3.) (D) Transverse section through anterior end of the mesonephric kidney of 10 mm. pig embryo presenting the Mullerian duct invagination of the coelomic epithelium covering the mesonephros. E -N are diagrams showing the adult excretory and reproductive duct relationships in various fishes. The urinary ducts are shown in black. (Redrawn and modified from Goodrich, 1930, Studies on the Structure and Development of Vertebrates, Macmillan and Co., Limited, London, after various authors.)

It will be observed that in the male ganoid fish, Acipenser, the vasa efferentia extend from a longitudinal testis duct through the anterior or genital part of the kidney to the Wolffian (mesonephric) duct. The Wolffian duct thus becomes a duct of Leydig as in the frog. However, in teleosts, and in Protopteriis and Polypterus, a separate genital duct which opens into the caudal end of the mesonephric duct is evolved. Hence, the Wolffian (mesonephric) duct in these forms functions as a urinary duct only. The separation of the genital duct from the urinary duct, with the exception of the urogenital sinus region at the posterior end, is a fundamental characteristic of most vertebrate male reproductive systems, including many amphibia. In female fishes, fig. 351, 1-N, as in other vertebrates, the reproductive duct is always distinct from the urinary duct. The exact homologies of the reproductive duct in forms such as Lepisosteus (Lepidosteus) and teleosts (fig. 351, L-N) with the Mullerian duct in other verterbates is not clear.

Fig. 351 — ( Continued)


See legend on pp. 798 and 799,


Fig. 351 — (Continued)

See legend on pp. 798 and 799.


35 1C). The blind caudal end of the invagination grows posteriorly along the side of the mesonephric duct to join the cloaca (fig. 351C-2).

a. Male Reproductive Duct

The developing gonad of the males of Amphibia, reptiles, birds, and mammals, together with the elasmobranch and ganoid fishes, appropriates the mesonephric duct for genital purposes. In this appropriation, the rete tubules of the testis unite with certain of the mesonephric tubules. The latter form the vasa efferentia or efferent ductules of the epididymis (fig. 351A-C). In teleosts, dipnoan fishes, and Polypterus, the marginal testicular duct becomes modified into a vas deferens which conveys the genital products to the urogenital sinus (fig. 351F-H).

In all vertebrates and in some mammals (Chap. 1), the testis remains within the abdominal cavity. However, in most mammals and in the flatfishes, there is a posterior descent of the testis (figs. 3 and 5) into a compartment posterior to the abdominal cavity proper.

b. Female Reproductive Duct

In the eutherian or placental mammals, the two Mullerian ducts in most species unite posteriorly to form a single uterovaginal complex (fig. 349B, D). In all other vertebrates, the Mullerian ducts or oviducts remain separate (see figures 33; 351A-4, B-4). The vagina of the eutherian female mammal probably is constructed partly of entoderm from urogenital sinus, for entoderm from this area invades the caudal end of the uterovaginal rudiment and lines the vaginal wall, at least in part (fig. 349B, D).

In the teleost fishes (fig. 35 IM, N), the origin of the Mullerian ducts is problematical (Goodrich, ’30, pp. 701-705).

5. Development of Intromittent Organs

Various types of intromittent structures are described in Chapter 4. The development of pelvic-fin modifications under the influence of the male sex hormone occurs in fishes. Cloacal intromittent structures are developed in certain Amphibia. A definite penis occurs in reptiles, certain birds, and in all mammals. The transformation, occurring in the external genital structures in male and female human embryos, is shown in figure 349E-K.

6. Accessory Reproductive Glands in Mammals

Refer to figures 2 and 349C.

a. Prostate Gland

The prostate gland arises as entodermal outgrowths from the membranous urethra near the entrance of the genital ducts. The surrounding mesenchyme provides the connective tissue and muscle. The paraurethral glands or ducts of Skene in the female represent minute homologues of the prostate gland.

b. Seminal Vesicles

The seminal vesicles arise as saccular outgrowths from the mesonephric ducts.


c. Bulbourethral Glands

The bulbourethral (Cowper’s) glands in the male arise as outgrowths from the entoderm of the cavernous urethra. The vestibular glands or glands of Bartholin are the female homologues of the bulbourethral glands.

7, Peritoneal Supports for the Reproductive Structures a. Testis and Ovary

The testis and ovary are pendent structures in all vertebrates and they are ’ ’ ■extensions from the dorso-lateral region of the coelomic cavity. The support of the testis is the mesorchium and that of the ovary is the mesovarium. However, supports other than those mentioned in the preceding sentence are concerned with the support of the testis and ovary during development. Figures 3 A, B and 351C-3 demonstrate an anterior ligamentous, progonal support for the developing sex gland, whereas caudally there is a posterior, epigonal support continuing posterially to join the inguinal ligament of the mesonephros. In the developing mammal the progonal support merges with the diaphragmatic ligament of the mesonephros. Caudally the inguinal ligament of the mesonephros joins a ligamentous area in the genital swelling, known as the scrotal ligament in the male and the labial ligament in the female. Consult fig. 351C-6 and C-7 for later history.

b. Reproductive Ducts

The male reproductive duct (vas deferens, Wolffian duct) lies close to the kidney structures in the retroperitoneal space in most vertebrates other than those mammals with descended testes (see Chap. 1). The male reproductive duct, therefore, assumes a retroperitoneal position and is not suspended extensively within the coelomic cavity. On the other hand, the female reproductive duct (oviduct) is a pendant, twisted structure and is supported by a well-developed peritoneal support, the mesotubarium. In mammals, due to the fact that the reproductive ducts tend to join posteriorly, the mesotubarial supports, along the caudal region of the reproductive ducts, aid in dividing the pelvic region of the coelomic cavity into two general regions, viz., a dorsal or rectal recess, and a ventral, urinary recess (fig. 349L, M ).

In the mammals, the mesotubarial support of the Fallopian tube is known as the mesosalpinx. The mesosalpinx is continuous with the broad, shelf-like, lateral support of the uterus, known as the broad Ugament. The broad ligament is developed from the mesotubarium together with the remains of the mesonephric kidney substance (349L, M). The round Ugament of the mammalian uterus and the ovarian ligament arise from a basic rudiment comparable to the gubernaculum testis in the male (see figs. 3; 351C-3, C-6, C-7).


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