Paper - Development of the Mouse Gonads 2

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Brambell FWR. The development and morphology of the gonads of the mouse. Part II. The development of the Wolffian body and ducts. (1927) : 206-219.

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This historic 1927 paper by Brambell is the second in a series investigating the development of the mouse gonad.

See also: Brambell FWR. The development and morphology of the gonads of the mouse. Part I. The morphogenesis of the indifferent gonad and of the ovary. (1927) 101: 391-407.
Brambell FWR. The development and morphology of the gonads of the mouse. Part II. The development of the Wolffian body and ducts. (1927) : 206-219.
Brambell FWR. The development and morphology of the gonads of the mouse. Part III. The growth of the follicles. (1928) 103: 259-272.
Rowlands IW. and Brambell FWR. The development and morphology of the gonads of the mouse. Part IV. The post-natal growth of the testis. (1932) : 200-213.

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The Development and Morphology of the Gonads of the Mouse Part II. The Development of the Wolffian Body and Ducts

Francis William Rogers Brambell (1901 – 1970)

By F. W. Rogers Brambell, Lecturer in Zoology, King’s College, London.

James Peter Hill (1873 - 1954)

(Communicated by Prof. J. P. Hill, F.R.S. — Received August 4, 1927.)

(From the Department of Anatomy (Embryology and Histology), University College, London.)

[PLATES 13-16.]

1. Introduction

This paper is concerned with the embryonic development of the Wolffian body and duct, the Mullerian duct, and the urogenital connection in the mouse. Part I dealt with the development of the indifferent gonad and of the ovary after differentiation. The germinal ridge is first established in the embryo 9 days p.c., and the gonads are definitely difierentiated into ovaries or testes 12 days p.c. Parturition takes place 19 days 12.0., and sexual maturity is attained at about 8 weeks pp. In the mouse the mesonephros is vestigial and non-functional, a point that must be constantly borne in mind in comparing it with, for instance, such as the rabbit, in which the mesonephros is large, well developed and functional. The epithelial proliferation beginning in the forming germinal ridge and continuing, in the female, until after birth is not in the form of cords, but is continuous over the whole surface of the gonad, and gives rise to the solid epithelial nucleus. Furthermore, it is not divided into a medullary and a cortical proliferation, but is one single process. After the ovary is differentiated the epithelial nucleus is broken up, to a certain extent, into finger-shaped lobes or cords by the down-growth of mesenchyme from the hilum, but this process is entirely secondary.

In the male the epithelial proliferation and the solid epithelial nucleus continue until the tunica albuginea is formed at the time of sexual differentiation. Mesenchyme growing down from the hilum forms the tunica albuginea, and breaks up the solid epithelial nucleus into spermatic cords. The formation of the spermatic cords is, therefore, also secondary. These peculiarities of the mouse are probably associated with the small size and rapid development of the early gonad rudiments. They are of the iitmost importance in connection with the relations of the urogenital connections and ducts to the spermatic tubules in the testis and the homologous structures in the ovary.

The author would like to take this opportunity of expressing his thanks to Prof. J. P. Hill, F.R.S., for his advice and criticism in connection with this work, and to Dr. A. S. Parkes for much helpful criticism. The material for this research was purchased with the help of a grant from the International Education Board. The histological and photomicrogrsphic expenses were defrayed by a grant from the Government Grants Committee of the Royal Society. I wish to express my thanks for both grants.

2. Material

The material available consisted of 19 embryos from 9 to 12 days p.c., arranged in 9 stages, as the variation in the state of development necessitated a seriation not strictly in accordance with their ages. The material after 12 days 11.0. was taken at daily or half-daily intervals until birth. It consisted of 18 female embryos arranged in 8 stages and of 21 male embryos in corresponding stages. The series of material from birth to maturity consisted of 11 stages of each sex, covering each of the eight weeks.

The material was mostly fixed in Bouin's fluid and stained with Ehrlich's haematoxylin and eosin, or by Pasini’s method. Uomplete serial sections were made of the gonads or gonad regions in each case. excepting the larger testes. In addition, embryos at 12, 12}, 12}, 15 and 18 days 10.0; were dissected under a. dissecting microscope.

3. Description

The Differentiation of Sex

Sex can first be distinguished histologically in the mouse at 11.5 or 12 days E12. (5). It can be determined on micro-dissection easily at 13 days p.c. by the greater thickness of the testes as compared to the ovaries. By comparing micro-dissections of embryos from the same uteri, it was possible to distinguish the testes from the ovaries at 12; and 12 days 12.0. by the same method. At 12 days this distinction was not apparent. Measurements were made from the slides of the lengths of all the gonads of the ‘ embryos in the series between 11 and 13} days, inclusive. At the same time an outline drawing of the greatest cross-section of each was made with the aid of a camera lucida. The lengths of the gonads varied greatly, and were not correlated with sex. The area of the cross-sections was calculated with the aid of a planimeter, and the average of the two gonads of each embryo was plotted on the accompanying graph (text-fig. 1). It can be seen from this that the testes are perceptibly thicker at 11-} days, and are increasingly so at all subse- quent stages. In no case after sex can be distinguished histologically do the cross-sectional areas of the ovaries of any of the. females overlap those of the testes of the males from the same uterus. The apparent overlap at 12 days is not real, as the embryos from two uteri are plotted. Those from one uterus (Stage 7) are less developed histologically, and are all smaller than any of those from the second uterus (Stage 9). Drawings of micro-dissections of male and female 12% day p.c. embryos are shown in Plate 13, figs. 1 and 2. Similar In the testes the loops of the spermatic cords, attached to the mesotestis, can be seen as transverse ridges through the tunica albuginea. It is remarkable that the testes can be distinguished by measurement at the earliest stage at which they can be identified histologically, and that they can be told '34 hours lat er under a dissecting microscope or even with the naked eye.

The Wolffian Body and Duct at the Time of the Formation of the Genital Ridge.— This description begins with embryos of 9 days 11.0. at the stage when the first traces of the germinal ridge are forming. The development (and degeneration) of the Wolfiian body, the Wolffian duct and the Mullerian duct always proceeds strictly in an antero-posterior direction.

dissections at 15 days p.c. are shown in Plate 14, figs. 1 and 2.

In consequence, the stage of development of any one of these organs is usually noticeably more advanced at the anterior end than at the posterior end. In embryos 9 days 30.0. (Stage 1 (5) ) the Wolffian body is well established, and the tubules are formed anteriorly. The most posterior tubules are, however, not quite completely organised. The Wolflian duct is luminate throughout its length. Anteriorly it ends blindly just in front of the opening into it of the first mesonephric tubule. It measures approximately 35 to 40 p. in diameter. It may therefore be said that the Wolflian bodies and ducts are completely established at the time when the germinal ridges begin to form. Growth, however, continues in both for some time afterwards. At the next stage (11 days 12.0., Stage 3) 8 to 10 mesonephric tubules are found on each side. They are simple, slightly coiled tubules about 55 to 90 p. in diameter, with a small but definite lumen. Their wall is formed of a single layer of columnar epithelial cells with the nuclei away from the lumen. The tubules are without definite glomeruli, which are never developed, but rudimentary capsules in the form of slight swellings of the tubules are found in 11-day p.c. embryos. All the anterior tubules open into the Wolflian duct at regular intervals. but the posterior two or three do not, and are blind at both ends. There is no separation of the anterior and posterior tubules into groups, but it is possible that the anterior ones, opening into the Wolfiian duct, represent the epigonnl and the blind tubules the paragonal regions. The first tubules are slightly anterior to the epithelial nucleus of the gonad, and there are no tubules posterior to the anterior two-thirds of the latter. Each tubule ends close to the peri- toneal epithelium on the ventro-lateral aspect of the germinal ridge, the ends of those in the region of the gonad being only separated from the dorso-lateral border of the epithelial nucleus by a thin layer of mesenchyme. The extremities of the anterior tubules be attached to the ccelomic epithelium as nephrostornes, but it is impossible to be sure, in the single specimen of this stage, on account of the plane of sectioning being longitudinal, not tangential. N ephrostomial connections between the anterior tubules and the cmlomic epithelium are present in the embryo 10 days 12.0. (Stage 5 (5)).

Posteriorly it opens into the urogenital sinus.

Small funnel—shaped invaginations of the coelom are present in the most anterior nephrostomes, which are best developed. Three or four nephrostomes are anterior to the gonad, and a few, more diflicult to distinguish, are present at the dorso-lateral margin of the anterior portion of the gonad. At 11 days 13.0. (Stage 6 (5) ) better developed nephrostomes are present. About 3 occur anterior (Plate 15, fig. 1) to the gonad and 3 at least in the gonad region (Plate 15, fig. 2). In one embryo, a typical example, the ostium abdominale tubw (text- figs. 2 and 3) occurred 182 p. in front of the gonad. The first nephrostome (text-fig. 4) was 84 p. posterior to the ostium, the second 102 y., and the third 154 p., or 28 p. anterior to the gonad. The fourth was 21 y. posterior to the anterior pole of the gonad, the fifth 63 (J, and the sixth 147 p.. Traces of two more nephrostomes occurred behind the sixth. The two or three posterior tubules, which do not open into the Wolflian duct, have no nephrostomial connection with the coelomic epithelium.

In the clearest cases the nephrostomes are open and appear continuous with the lumina of the tubules ; in others they consist merely of solid connections between the peritoneal epithelium and the tubules. The ventral borders of the nephrostomes in the gonad region, immediately beneath the coalomic epithelium, are either in contact with the dorsal margin of the epithelial nucleus of the gonad or are only separated by a very thin layer of mesenchymal tissue. These nephrostomes are destined to participate in forming the rete testis or the rete ovarii, as the case may be. They remain unchanged in both sexes until 12 days pm. It has already been stated that glomeruli as such are absent in the mesonephros of the mouse, but rudimentary capsules of Bowman are represented by 3 slight swelling of the distal end of each tubule just before it joins the nepluostome. This swelling is slight but distinct, and its lumen is a little larger than that of the tubule just above it. Its wall is similar to the rest of the tubule.

Text~F1gs. 2-4.

(X 135. See description of Plates for key to reference letters.)

The cephalic portion of the Wolflian body anterior to the gonad becomes much reduced by the 12th day 12.12., and hardly projects at all in front of it. This reduction is partly apparent, owing to the unequal and relatiively enormous growth of the gonal region, and partly real, owing to atrophy of the pregonal region. In consequence, at the time when the urogenital union is efiected, all the nephrostomial rudiments are grouped about the anterior and of the gonad, and the ostium abdominale tuba is just in front of the anterior pole of the gonad.

The Urogenital Union of the Male

In the male the urogenital connection is effected slightly earlier than in the female. In the male embryo 12 days 39.9, (Stage 9 (5) ) the nephrostomes have ceased to communicate with the coslom, and the nephrostomial canals are becoming separated by mesenchyme from the coelomie epithelium. At the same time the epithelial nucleus is becoming «liiferentiated into definite spermatic cords by the down-growth of mesenchymal tissue from the primitive hilum. These spermatic cords are attached along the line of the hilum. The nephrostomial canals lie in close apposition to the hilar insertions of the forming spermatic cords, and are only separated from them by a thin layer of mesenchyme. As the nephrostomial canals become separated from the ceelomic epithelium they unite with the spermatie cords and constitute the urogenital connection.

The actual union seems to be efiected before the nephrostome is completely separated from the coelomic epithelium by a small down-growth from the ventral surface of the nephrostomial canal, near its junction with the epithelium (Plate 15, fig. 3). This down-growth breaks through the thin layer of mesen- shyme, separating it, and fuses with the spermatic cords. This connecting strand is small, and consists of only a few cells, as can be seen from the figure. It appears to be formed by a definite down—growth from the nephrostomial canal just distal to its coelomic opening. At this stage the rudimentary capsules of Bowman are so degenerate as to be indistinguishable from the nephrostomial canals on the one side and the mesonephric tubules on the other. It is thus impossible to define accurately the extent of the remains of the capsules. In consequence, it is possible that cells which previously formed part of a Bowman’s capsule may enter into the formation of the strand of cells which grows down from the nephrostomial canal and unites with the spermatic tubules. It would appear more probable, however, that the strand is formed as described from the elements of the nephrostomial canal alone.

The union is assisted by the constriction of the primitive hilum to form the mesorchium. This is efiected by the formation‘ of a lateral groove between the Wolflian body and the dorsal margin of the testis, which deepens and displaces the nephrostomial canals from the lateral margin towards the mid-line of the testis, and brings them into closer contact with the dorsal extremities of the spermatic cords.

The primitive nephrostomial canals, together with small down-growths from them, therefore appear to give origin to the definitive rete testis and, by acquiring an early, but secondary, connection with the spermatic cords, unite them to the anterior mesonephric tubules which open into the Wolffian duct. The posterior tubules, which never developed_ nephrostomial rudiments, do not contribute to the urogenital connection. The rete testis consists of a bundle of about seven fine tubules running from the testis through the anterior portion of the mesorchium to the anterior end of the Wolliian body. The lumina of the rete tubules remain incipient for some time, but become more marked by 14 days p.c. and are open at birth.

It appears that all the six to eight nephrostomial canals that are formed take part in the urogenital union. They are at first separate and distinct. Soon the constriction of the mesorchium presses them closer together and they then anastomose, forming a closely interwoven cord extending forward from the testis through the anterior margin of the mesorchium to the cephalic or epididymal portion of the Wolfiian body. The increase in the number of spermatic cords results in the ends of the rete becoming branched to unite with them.

These branches constitute the straight tubules of the testis, the tubuli recti. They are formed in part from the rete, but may be contributed to also by the hilar ends of the spermatic tubules. They do not exist as such at the time when the urogenital union is effected, but are developed before birth to deal with the increased number of spermatic tubules. They arise thus as a secondary difierentiation of the region of junction between the spermatic tubules and the rete. At 18 days p.c. their lumina are Well formed and much larger and more distinct than those of the rete. At this time the spermatic tubules are not yet luminate.

The connective-tissue sheaths of the spermatic tubules, which were derived from the down-growth of mesenchyme from the hilum, unite to form a sheath around the tubuli recti and rete. This sheath is augmented by the continued down-growth of connective tissue from the hilum and forms the mediastinum testis.

The vessels of the testis pass through the mesorchium immediately behind the rete cords (Plate 16, fig. 1).

The Urogenital Union in the Female.— The urogenital connection in the female is established slightly later than in the male. It is effected in an exactly similar manner. The female embryo at 12} days p.c. is at the same stage in this respect as the male embryo at 12 days 12.0. At this stage. the small ventral down-growths from the nephrostomial canals are passing into continuity with the epithelial nucleus of the gonad, and the nephrostomes are loosing their connection with the coelomic epithelium. This process, as in the male, is slightly more advanced in the anterior nephrostomial canals than in the more posterior ones. At this time the mesenchyme of the hilum is beginning to grow down into the epithelial nucleus and to split it up into epithelial cords. These down- growths constitute the primordia. of the connective tissue of the septa ovarii. At 131} days 12.6. the septa have extended from the hilum as far as the periphery of the ovary. The division" of the ovarian epithelial nucleus into epithelial r..'ords is, therefore, like the formation of the spermatic cords in the male, a‘ secondary process. The retia primordia effect their union with these epithelial cords at the time when they are just forming. The urogenital union in the female mouse is thus effected in a manner strictly homologous to that in the male. The constriction of the mesovarium, by the formation and deepening of a lateral groove along the line of junction of he ovary with the Wolflian body, assists in bringing about the urogenital union, in the same manner as the constriction of the mesorchium in the male.

The primitive nephrostomial canals and the down-growths from them therefore give origin to the definitive rete ovarii and unite the epithelial cords to the anterior mesonephric tubules. At the time when the union is effected the anterior mesonephric tubules open into the Wolfiian duct. The posterior tubules, which, as in the male, never develop nephrostomes, do not contribute to the urogenital connection. The rete ovarii thus consists primarily of a bundle of about eight fine tubules running from the ovary through the anterior portion of the mesovarium to the anterior end of the Wolffian body. The lumina remain incipient until about the 18th day 12.6., when they become open.

It appears that, as in the male, all the nephrostomial canals take part in the formation of the rete. They are at first separate and distinct, but soon anastomose with each other.

The hilar portions of the septa ovarii, augmented by a further down-growth of mesenchymatous connective tissue from the hilum, ensheath the ovarian portion of the rete and their junctions with the epithelial cords. This forms the mediastinum ovarii, the homologue of the mediastinum testis.

The vessels of the ovary pass through the mesovarium immediately behind the rete cord (Plate 16, fig. 2).

The Later Development of the Wolffian Body and Duct in the Female

The down-growth of connective tissue from the hilum which contributes to the formation of the mediastinum ovarii continues, and forms a central knob of tissue in the ovary by the end of gestation. This knob of tissue constitutes the primitive medulla. It includes the ovarian portion of the rete. As development proceeds the medulla. is contributed to by the inner ends of the epithelial cords, in which the germ-cells have degenerated. The rete tubules loose their definite connections with the epithelial cords of the definitive cortex during this process of medulla formation. They persist, however, during adult life as a number of isolated cords in the medulla.

In the female the Wolflian duct degenerates early. At 14 days 13.0. the anterior end shows signs of degeneration, at 15 days 13.0. it has degenerated throughout the ovarian region. The degeneration proceeds from before backwards.

The anterior mesonephric tubules, about 8 in number, which at first unite the rete with the Woltfian duct, constitute in the female the epoophoron (Plate 16, fig. 2). They loose their connection with the Wolfiian duct as soon as it begins to degenerate. Subsequently they persist, without developing further, as a few blind tubules to which the retc tubules are attached, and which can be detected in the mesovarium of the adult female.

The blind posterior tubules, one or two in number, which do not take part in the urogenital connection, constitute the paroophoron. Like the para- didymis in the male, it degenerates early and cannot be detected at birth.

The Early Development of the Mullerian Duct.——There are no traces of the ostium abdominale tubes to be found in the embryos earlier than 10 days 11.0. (Stage 5 (5) ). At 10 days 13.6. a varying number of rudimentary nephrostomes in connection with the nephric tubules are to be found in the region where the ostium will be developed. It is impossible to distinguish the primordium of the ostium from the other nephrostomes. At the next stage (Stage 6 (5)), 11 days 32.0., the ostium can be distinguished from the nephrostomes. It consists of a groove or funnel in the ventral side of the urogenital fold, and is situated on a level with the extreme anterior end of the Wolffian duct. Except for its somewhat larger size and the absence of any connection with the mesonephric tubules, it closely resembles in structure and position the true nephrostomes. It is 84 p. anterior to the first nephrostome and 182 p. anterior to the’ gonad. At 12 days 37.0. (Stage 9 (5) ) the ostium abdominale tubae has deepened. Its iree extremity extends up beneath the lateral epithelium of the urogenital fold almost to the level of the Wolffian duct, and proceeds to grow backwards beneath the peritoneal epithelium immediately superficial to the Wolfiian duct.

The rapidly growing tip exhibits many mitoses. It is closely applied to the overlying peritoneal epithelium in a manner which suggests that the latter is adding to it by proliferation. The absence of mitoses in this region of the peritoneal epithelium, however, precludes this possibility. The rapid backward growth of the tip of the ostium abdominale tubze to form the Mullerian duct continues until it extends into the genital cord, which has been formed already by the union of the two urogenital folds. This origin is exactly similar to that described in the human embryo by Felix (7). He says : “ Its growth results entirely from its own forces, the outgrowing tip being always free, and connected neither with the cualomic epithelium nor the primary excretory duct; only poorly preserved or poorly fixed preparations could deceive one on this point. The growth depends on the increase of cells partly along the entire extent of the duct, as is shown by the mitoses, partly at the outgrowing end, which is frequently swollen and presents all the peculiarities of a so-called cone of growth.”

The development of the Fallopian tubes and the ovarian capsules in the mouse is described in detail by Agduhr (1).

The Degeneration of the M iillerian Duct in the M ale.—In the male the Mullerian duct degenerates early. Degeneration begins in the anterior end and proceeds caudalwards. At 12.} days 12.0. the development of the Mullerian duct in the male is exactly similar to that in the female, and the development of the posterior region continues in the same manner until 13:} days 32.0. Degenerative changes are first observable in the cephalic end of the duct, opposite the anterior pole of the testis, at 13 days 11.0. At 13; days p.c. the ostium abdominale tube: is reduced to a mere blind groove, and the anterior portion of the Mullerian duct has disappeared. Farther back, opposite the posterior half of the testis, the duct is present, but is small and shows signs of degeneration. Posterior to the testis the duct is at the same stage of development as in the 13-day p.c. female embryo. The Wolflian duct is, however, larger and better developed throughout its length than the Mullerian duct.

At 15 days 33.0. the degeneration of the Mullerian duct in the male is more advanced, and at 16 days 71.0. it has almost disappeared in the testis region. The mesenchyme around the Mullerian duct which forms the ridge that, in the female, would develop into the muscle layers of the uterus, degenerates also. It first becomes arranged loosely around the duct and then gradually disappears. The degenerative changes set in so early in the male that the anterior end of the duct has disappeared before the posterior end has reached its maximum development.

4. Discussion

Many views have been put forward regarding the origin of the rete in both ovary and testis. A large number of workers, including de Winiwarter and Sainmont in the cat (11), and de Winiwarter in the rabbit (10) and man (1:2), consider that outgrowths from the walls of the Malpighian corpuscles unite with the sex-cords and give origin to the rete tubules.

Other workers, including Allen (2) in the pig and rabbit, and in Chrysemys (3) trace the rete to peritoneal invaginations. Allen (3) states that the rete in Chrysemys is formed by the union of “ funnel-cords ” (nephrostomial canals) with evaginations from the capsules of Bowman. The funnel-cords are derived from the “ peritoneal funnels ” (nephrostomes) of the Malpighian corpuscles. He is inclined to consider the funnel cords as modified sex-cords. Fraser (8). in the Marsupials, describes the origin of the rete from a core of cells lying within the genital ridge anterior to the germinal rudiment. She considers that in Perarneles, and probably also in Trichosurns and other marsupials, the core of cells within the genital ridge is derived from the nephrostomial canals of the mesonephros, which loose their connection with both the ccelomic epithelium and the Malpighian corpuscles, and unite into a continuous mass of cells. Reference should be made to this paper for a bibliography of the subject. Van Beek (4) also traces the rete to the pre-gonal germinal ridge.

Felix (7), and recently Wilson (9), consider that the rete in the human subject originates from the deeply lying cells of the early gonad. This rete blastema, therefore, is of coelomic epithelial origin. The rete, on this view, is not derived from the Wolfiian body, and the union with the Malpighian corpuscles, or evaginations from them, is secondary. De Burlet and de Ruiter (6) have maintained that, in the mouse, the rete is formed from the longitudinal core (Ldngstamm), to which the spermatic tubules are attached, and the epithelial ridge (Epithelkamm) attached to it. Agduhr (1). however, maintains that. in the mouse, the rete is formed by the down-growth of epithelial cords from the cranial end of the genital ridge.

The material described in this paper shows that a nephrostomial funnel is formed in connection with each of the mesonephric tubules, which will ultimately form part of the epididymis or epoophoron. These funnels, open or closed, are situated immediately dorso-lateral to the anterior portion of the gonad, in the stage immediately before the urogenital connection is established. The end of the mesonephric tubule with which the funnel unites is sometimes slightly swollen to form a rudimentary capsule of Bowman, but no glomerulus is formed in connection with it. At the next stage the capsules of Bowman an diflicult to define, and more or less indistinguishable from the nephrostomial canal on the one side and the mesonephric tubule on the other. The nephrog. tomial canals are becoming detached from the peritoneal epithelium, and at. the same time they are united with the epithelial nucleus of the gonad by strands of cells. These strands appear to grow down as a solid evagination from the ventral side of the nephrostomial canal at a point close to its coalomic extremity.

If these strands of cells are formed from the elements of the degenerate capsules of Bowman, the condition in the mouse is homologous to that described in other animals by dc Winiwarter. On the other hand, if they originate from the nephrostomial canals, as appears more probable, the condition is akin to that described by Allen and Fraser. It differs from the latter author's chiefly in that the rete is formed in the gonad region from nephrostomial rudiments formed immediately dorso—lateral to it, and not from the region of the urogenital ridge anterior to the gonad. It is obvious that the rete tubules are primarily united with the mesonephric tubules, and that the union with the germinal elements is secondary. These findings are therefore distinctly contrary to those of Felix and Wilson.

The method of formation of the urogenital connection in the mouse, although simple in itself, is thus extremely diflicult to interpret in the light of other mammals. This is due to the small size and rapid development of the gonads of the mouse and the vestigial nature of the Wolffian body.

In View of the fact that, in the mouse, the epithelial proliferation in the gonad is not, at first, in the form of cords, no conclusion can be drawn as to the homology of the nephrostomial canals and the “ sex-cords ” described in other forms. In the mouse the mesenchyme does not appear to contribute to the urogenital union itself, but its down—growth into the gonad results in the formation of the mediastinum and breaks the epithelial nucleus of the gonad 11p into spermatic or ovarian cords.

No connection was observed between the suprarenal primordia and the nephrostomes, such as has been described by Fraser and other authors. Indeed, as these, in the mouse, are widely separated by the gonad, the suprarenal anlage being median to it, and the nephrostomes lateral, no relation between them could exist.

The Mullerian duct develops, as stated by Felix (7) and de Winiwarter (12), in the human species, as a back-growth of the inner end of the ostium abdomin ale tuba}. The similarity in structure of the primordium of the ostium abdominnle tabla to the nephrostomes, and its similar position in the urogenital ridge slightly anterior to them, suggests that they may be homologous. On this view the ostium abdominale tubes would be a nephrostome which grew and extended posteriorly to form the Mullerian duct.

5. Summary

  1. The differentiation of sex is accompanied from the beginning by an increase in diameter of the testes as compared to the ovaries. This can be detected by comparing the cross-sectional areas of the gonads of embryos from the same uterus at and after 114} days 11.0. It can be detected in micro—dissections at 12} days 11.0.
  2. The mesonephros of the mouse is small and non—functional. It is composed of about ten mesonephric tubules. No glomeruli are formed, but rudimentary capsules of Bowman are represented by slight swellings on the distal ends of the tubules. About eight of the most anterior of these latter are connected with the peritoneal epithelium, immediately dorso-lateral to the gonads, by nephros— tomial canals.
  3. The urogenital connection is effected by the down-growth of strands of cells from the nephrostomial canals which fuse with the epithelial nucleus of the gonad and form the rete. The connection is established in the male at 1:} days 12.0., and slightly later in the female.
  4. The six to eight tubules united with the gonad by the rete cords form the epididyrnis or epoophoron. The blind posterior tubules form the paradirlymis or paroophoron ; they degenerate completely.
  5. The ostium abdominale tubaa arises as an invagination of the peritoneal epithelium into the urogenital ridge anterior to the gonad and nephrostomes. It is suggested that it may be homologous to the mesonephrostomes.
  6. The Mullerian duct is formed by the growth backwards of the inner end of the ostium abdominale tubae;


(1) Agduhr. Acts. Zool.. vol. 3 (1927).

(2) Allen BM. The embryonic development of the ovary and testis of the mammals. (1904) J. Anat. 3(2): 89-154.

(3) Allen. B. M., Amer. Jour. Anat., vol. 5 (l905—6).

(4) Van Beek. Zeits. fur die Gesamte Anat., Abt. 1, vol. 71 (1924).

(5) Brambell, Roy. Soc. Proc., B, vol. 101 (1927).

(6) de Burlet and de Ruiter, Anat. Hefte, Be-itriige, vol. 59 (1920).

(7) Felix W. The development of the urinogenital organs. In Keibel F. and Mall FP. Manual of Human Embryology II. (1912) J. B. Lippincott Company, Philadelphia. pp 752-979.

(8) Fraser EA. The development of the urogenital system in Marsupialia, with special reference to Trichosurus vulpecula. Part II. (1919) J. Anat. 53: 97-129. PMID 17103868

(9) Wilson, Carnegie Inst. Washington, Contributions to Embryology, vol. 17 (1926).

(10) de Winiwarter, Arch. de Biol., vol. 17 (1900).

(ll) de Winiwarter and Sainmont, Arch. de Biol., vol. 24 (1909).

(12) de Winiwarter, Arch. de Biol., vol. 25 (1910).

Description of Plates

Guide Letters

A., Aorta. A.m.s., A. mesenterica superior. A. umb.. A. umbilica. B., Bladder. B.V., Blood vessel. C., Ovarian cortex. D., Diaphragm. E.T., Tubule of epididymia or epoophoron. G.C.. Genital cord. G.R., Germinal ridge. G.T.. Genital tubercle, K., Kidney. Lig. 0., Ligamentum ovarii. Lig. T., Ligamentum testis. Medulla of ovary. M.C‘., Rudimentary capsule of Bowman. M.D., Miillerisn duct. Mess. j., Mesonephric fold (tubal portion). M.T.. Mesonephric tubules. N., Nephros- tome. 0., Ovary. O. abd., Ostium abdominale tubaa. Pl. d.. Plica diaphragmatica. Pl. ing., Plica inguinalis. P.R.. Pre-gonal region of urogenital fold. R., Rectum. R.t., Rete tubules. S.. Ridge formed by the developing suprarenal and kidney. Supr., Suprarenal. S.T._. Spermatic tubules. T., Testis. T.R., Tubuli recti of testis. Ur., Ureter. V.c.i._. V. cava inferior. V.h.a., V. hemiazygos. W.D.. Wolllian duct.


l.—Dissection’of l2§-day pm. 52 mouse embryo. The long narrow ovaries are seen attached to the small mesonephric fold. Medial to each ovary is a swelling in the body wall produced by the developing suprarenal bodies and the kidneys. The cephalic extremity of each mesonephric fold, showing the ostium abdominale tubes, is attached to the diaphragm, which is cut across, by the short plica diaphragmatica. X15}.

2.—Dissection of 12}-day p.c. 3 mouse embryo. The testes are much thicker in proportion than the ovaries of the S.’ embryo from the same uterus (fig. 1). The loops of the spermatic tubules can be seen as slight ridges on the surface of the testis on the right-hand side of the picture. The ureters are seen as two ridges on the dorsal body wall, and the inguinal folds are clearly visible. Ex’ 22.

Pure 14.

l.—Dissection of 15-day p.c. 9 mouse embryo. The ovaries are being pushed laterally by the developing kidneys, which are now distinguishable from the supra- renal bodies. The plica diaphragmatiea is long. The ostium abdominale tubes is clearly visible. The ligamentum ovarii and plies. inguinalis are clearly shown. The junction of the tubal portions of the two znesonephric folds to form the genital cord is visible just in front of the bladder. In this specimen only one umbilical artery could be distinguished. x 13}.

2.—Dissection of 15-day p.c. a‘ mouse embryo. The testes are much larger and more ovoid than the ovaries of the female embryo from the same uterus (fig. 1). The loops of the spermstic cords can be seen as ridges on the surfaces of the testes. The testis on the right of the picture is approximately in its original position, but that on the left is undergoing a. torsion about the mesonephric fold and is also being displaced laterally by the developing kidney. X 17}.


l{1‘y_dey_j:.e.-emhuyo. x 450. _ ; _3.é—Dnwing of I nephroetome at the anterior end of the gonad of an 11-day p.c. -. ' X 450. _ -' H ‘3,.—Dxe.wing of enephmetomial canal in the gonal-region of a 12-day p.c. J embryo. The rudimentary capsule of Bowman can be seen. Between it and the peritoneal epithelium a. narrow down-growth connects the nephroetomial canal with the testis. This is the primordium of a. xete tubule. X 450.

l. Section of testis of 18-day p.c. mouse embryo, showing the zeta, tubuli recti; epididymie, and vascular supply. X 112.

2. Seetion of ovary at 18-day p.c. mouse embryo, showing the rete, developing medulla, epoophoron and vascular supply. x 112.

I am indebted to Mr. A. K. Maxwell for the drawings reproduced in Plates 13 and 14, and to Mr. F.» J. Pittook for the photomicrographs reproduced in Plate 16.