Paper - The histology of an hermaphrodite pig and its developmental significance (1929)

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Brambell FW. The histology of an hermaphrodite pig and its developmental significance. (1929) J Anat. 63: 397-407. PMID 17104239

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This 1929 paper by Brambell describes the abnormal genital development in the pig.



Modern Notes: genital abnormalities | pig



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The Histology of an Hermaphrodite Pig and its Developmental Significance

By F. W. Rogers Brambell

Lecturer in Zoology, King’s College, London

(From the Department of Anatomy (Histology and Embryology), University College and the Department of Zoology, King’s College, London)

I. Introduction

The example described in this paper is essentially similar to many of the pigs exhibiting hermaphroditismus verus lateralis described by Pick) and other authors, and more recently by Baker (1, 3) in this country. The gross anatomy presents no points of importance which have not been recorded by these authors and therefore only requires brief description. The histology of the ovotestes of such pigs has not received, however, adequate attention although it merits accurate description. This aspect, in the present instance, is of prime importance, since it reveals several facts of considerable interest and of theoretical significance, such as the presence of a cortical zone of spermatic tissue outside the tunica albuginea, the tubules in which open on the peritoneal surface by pores, and the occurrence of true oocytes in spermatic tubules. The author is indebted to Mr A. S. Foster through whom the material was obtained, and to Prof. J. P. Hill, F.R.S., and Mr J. R. Baker for valuable criticism and advice. The histological expenses were defrayed from a grant from the Government Grants Committee of the Royal Society for. which the author’s thanks are due.

II. Description

General description

The material described was removed from a young pig, about six weeks old, as gonadectomy is customary with animals intended for bacon. The gonads and associated structures were then dropped intact into a bottle of Bouin’s fluid in which they remained until they were received by the author some days later. It is understood that the external genitalia of the pig in question were abnormal in character, and that similar cases have occurred before on the same farm. Unfortunately no other information, apart from that derived from the fixed material, is available.


The material consists of the two gonads and epididymides, the two uterine cornua and part of the median portion of the uterus and two vasa deferentia. The right gonad, which was the smaller, proved to be an ovotestis. It measured about 17 mm. in diameter and was rounded almost spherical in shape (textfig.1). The left gonad was a testis and measured 22 mm. in diameter (text-fig. 2). Both gonads presented a firm smooth surface like that of a normal testis and each was attached by a broad hilum (Plate I, figs. 1 and 2). The epididymides were large, convoluted and roughly L-shaped, that on the left being somewhat larger than the right. The hilum of the testis was attached to the longer arm of the L in the angle of each epididymis. A pampiniform plexus was present on each side attached to the epididymis (Plate I, figs. 1 and 2). Sections showed that the tubules of the epididymides were empty and devoid of spermatozoa (Plate I, fig. 3).


Text-fig. 1. Right gonad, showing ovarian patch

Text-fig. 2. Left gonad showing the convoluted on testis. T, testis. OV, ovary. H, epididymis. tip of the oviduct and the pampiniform OD, oviduct. VD, vas deferens. The double plexus, PP. Other letters as in text-fig. 1. dotted line across the gonad indicates the x 12. plane of section. x 1-2.


The uterine cornua and vasa deferentia were attached to the outer sides of the angles of the epididymides (text-figs. 1 and 2). The uterine cornua were much convoluted and measured approximately 3 to 8-5 mm. in diameter throughout the greater part of their length. They tapered to a point on the surfaces of the epididymides, to which their extremities were closely attached, and the extremity of that on the left was convoluted (text-fig. 2), while that on the right was straight. The median uterus, close to the point where the two cornua fused, measured 3-5 mm. in diameter. The uteri, though small, were well developed and the mucosa was thick and full of glands (Plate I, fig. 4). The vasa deferentia, after leaving the epididymides, extended back on each side, parallel to the cornua in the uterine mesentery. They were applied to the ventral wall of the median uterus on each side and embedded in the substance of the - broad ligament. They were well developed, 370 in diameter on an average, but their lumena contained no spermatozoa. More detailed description of the anatomy seems unnecessary in view of the excellent descriptions by Baker (1, 3) of similar cases.

The fixation in Bouin’s fluid was good, but would have been better had the material ‘been cut into pieces before fixation. Staining with Ehrlich’s haematoxylin and eosin, Pasini or van Gieson gave good results.

Structure of the gonads

The ovarian portion of the ovotestes of pigs always occurs in a definite position in relation to the testis and epididymis. It is invariably situated on the pole of the testis next the angle of the epididymis. Accordingly this region of both gonads was sectioned aswell as other parts. No ovarian tissue nor any oocytes could be found in the left gonad which was otherwise identical in structure with the right. The following description, with this reservation, applies equally to both gonads.


The major part of each gonad consists of a central testis surrounded by a well-developed tunica albuginea of fibrous connective tissue, which is, in many places, 80 to 110 thick. This central spermatic tissue consists of numerous lobules separated by connective tissue trabeculae in which the larger vessels run (Plate IT, fig. 5). Each lobule is composed of numerous small tubules lined by a simple epithelium which obliterates the lumen and exhibits no signs of spermatogenesis. Quantities of large glandular interstitial cells in islets and strands, and a connective tissue network with capillaries, fill up the interstices between the tubules.


Outside the thick tunica albuginea is a narrow cortical zone of tissue which surrounds the entire gonad except in the region of the hilum. The greater part of this zone is composed of spermatic tissue with tubules resembling those in the medulla, interstitial cells, etc. This testicular cortex attains a thickness of 550 in places (Plate II, fig. 2) and is surrounded by a thin fibrous connective tissue layer, forming a poorly developed tunica albuginea about 10, thick. At the pole next the angle of the epididymis this testicular cortex in the right gonad passes into a patch of ovarian tissue about 2:5 mm. in diameter, and 1-25 mm. thick, which is composed of typical ovarian stroma containing many small oocytes in primordial follicles (Plate II, figs. 1 and 4). No large follicles or corpora lutea are present. The external tunica thins out and merges with the fibrous stroma in this region, and it is covered by a cubical peritoneal or germinal epithelium, which does not extend over the spermatic portion. The chief or medullary tunica extends beneath the ovarian region, between it and the central testis (Plate II, fig. 4), but is here somewhat broken and less distinct than in other places. The transition zone between the ovary and the cortical spermatic tissue is intermediate in character and contains ovarian stroma and tubules with oocytes in them (Plate II, fig. 3).


The ovary passes over on one side into the fibrous tissue of the hilum containing the rete testis, vascular supply and lymph lacunae.


The left gonad is identical in structure except that the cortex is entirely spermatic in character, no ovarian tissue having been discovered, even in the most likely region.


The medullary region. The lobules of the medulla measure about 1 mm. in diameter and are separated by stout trabeculae of fibrous connective tissue, often 50, in thickness, which are well supplied with blood vessels. The tubules (Plate II, fig. 5) in the lobules are small and convoluted; they measure about 50 to 70, in diameter on an average. Each has a thin, but distinct, connective tissue basement membrane and a lining of a single layer of epithelial cells, the cytoplasm of which completely fills the lumen of the tubule. These cells occasionally exhibit mitoses, are not distinguishable into sertoli cells and spermatogonia and never exhibit prophase stages. Their nuclei are more or less oval in shape and their outline is somewhat irregular. The tubules in the different parts of the medulla are all in the same stage of development.


The interstitial cells are large and glandular in appearance and stain densely. They are roughly polygonal in shape and the nuclei are usually eccentric. The illustration (Plate IT, fig. 5) shows that they are very plentiful and fill up the interstices in the fine network of connective tissue which occupies the spaces between the tubules. Both tubules and interstitial cells are of the type commonly found in undescended testes.


The tunica albuginea surrounding the medullary region is dense and thick. It is composed of fibrous connective tissue and is similar to that surrounding a normal testis (Plate II, figs. 2 and 4).

The ovarian cortex. The stroma in the deeper portions of the ovarian tissue is dense and fibrous and contains numerous lymph lacunae. The more superficial stroma is less fibrous and some of the cells are epithelial in appearance. It is well supplied with capillaries and lymph lacunae. Its surface is covered by a cubical peritoneal epithelium similar to that of a normal ovary. Numerous oocytes are present in primordial follicles consisting of a few flattened epithelial cells. They are localised chiefly in the superficial region, and are less frequent in the deeper parts (Plate II, figs. 1 and 4). These oocytes range from 25 to 35 in diameter and therefore have not entered on the growth stage. They are normal and healthy in appearance with smooth cytoplasm and plump nucleus. The nuclei of the majority have attained the typical resting stage of the prophase of the heterotypic division. Some of the nuclei, however, exhibit polarised loops which have not yet been transformed into the reticulum of the resting stage. No larger oocytes or follicles are present.


The ovarian region merges gradually with the testicular cortex. The transition zone presents some of the characters of both the testicular and ovarian regions of the cortex. It is composed of stroma similar to that of the ovary and of tubules and follicles interspersed with each other. The interstitial cells are not plentiful in this region. The follicles contain normal oocytes similar to those in the truly ovarian tissue (text-fig. 3). The tubules are indistinguishable from those in the definitely spermatic region of the cortex. Many of the tubules in the immediate vicinity of the ovarian tissue contain scattered oocytes (Plate II, fig. 3). These oocytes occurring actually in the tubules (text-fig. 6) are exactly similar to those in the ovarian cortex and some of them also exhibit polarised chromatinic loops in the nuclei. These oocytes present a definite and distinct outline and nucleus. Their nature is quite indisputable and they cannot be confused with the deceptive ovum-like bodies described by Crew and Fell(7), and said to be formed by a process of colloidal degeneration. Moreover, stages can be found in this region in which oocytes occur in “follicles”? which are intermediate in structure between the tubules and the primordial follicles (text-figs. 4 and 5). The oocytes in tubules are strictly limited to this narrow transition zone between the ovarian and testicular cortex (Plate II, fig. 4).



Text-figs. 3-6. Drawn with the aid of a camera lucida. x 600. Fig. 3 shows an oocyte in a normal primordial follicle from the ovarian region. Figs. 4 and 5 show oocytes in enlarged follicles. resembling tubules from the intermediate zone between the ovarian and spermatic portions of the cortex. Fig. 6 is from this zone also and shows three oocytes in a spermatic tubule.


The peritoneal epithelium rapidly thins and disappears over the transition zone and its place is taken by the thin cortical tunica albuginea which is continuous with the ovarian stroma and which surrounds the testicular cortex, merging with the thicker medullary tunica albuginea only in the region of the hilum where no cortex is developed.


The testicular cortex. The thin testicular cortex varies considerably but attains a thickness of 550 at the pole of the gonad farthest from the ovarian region. The tubules are similar to those in the medulla in structure except that the cytoplasm of the lining epithelium is less dense and more vacuolated (Plate II, fig. 2). The nuclei of these cells are similar to those in the medullary tubules in size and appearance and in the way they are arranged in a single layer near the wall of the tubule. They occasionally exhibit mitoses but never enter on the heterotypic division. The majority, if not all, of these tubules open on the peritoneal surface of the gonads by distinct pores (Plate II, fig. 2). These pores perforate the thin cortical tunica albuginea and the wall of the tubule. Sometimes they open directly into a tubule, when it is near the surface, and sometimes by a short but distinct canal (Plate II, fig. 2). The pores are quite distinct and may be marked either by a small extrusion of, or a hollow in, the contents of the tubule. The margins of the pores are clear cut and distinct in some instances, and ragged in others. Their definite structure and regular appearance preclude the possibility of their artificial formation during fixation or the subsequent treatment. The tubules branch and ramify in the cortex and are frequently more or less perpendicular to the surface; some, however, lie close to and parallel with it. This arrangement results in their being cut longitudinally more frequently than the tubules in the medulla and they consequently appear longer.


The tissue between these tubules is composed of loose fibrous connective tissue, containing many capillaries, lymph lacunae and strands and groups of interstitial cells. The latter are apparently identical with those in the medulla, but are not so numerous or so densely packed. The tubules are never grouped in lobules at the periphery, but incipient lobules are seen occasionally in the deeper layers immediately outside the medullary tunica or even forming islets surrounded by it. Such lobules are indistinguishable from those in the medulla. The Histology of an Hermaphrodite Pig 403

III. Discussion

Morphological significance

The gonads described in this paper are chiefly of interest because of the light they throw on the origin and development of hermaphroditism. The presence of a medulla and cortex, separated by a tunica albuginea, is one of their most remarkable characteristics. Baker(1) evidently observed a similar arrangement, since he notes and figures the occurrence of spermatic tubules outside the tunica albuginea in intersexual pigs. It must be assumed that the medulla represents the testis of a normal male, and that its tubules have been derived from the first or medullary cords proliferated during embryonic life from the germinal epithelium. The tunica albuginea surrounding the medulla must be homologous with that surrounding the normal testis and therefore represents the primitive tunica albuginea of the embryonic gonad which persists in the male but disappears in the female. The zone outside this tunica will, on these assumptions, be homologous with the cortical cords which form the cortex of the ovary but do not develop in the normal male. This zone obviously has been arrested at an early stage and has never attained as full a development as in the normal ovary. The small ovarian portion alone has completed its differentiation and produced typical ovarian tissue. The tubules composing the remainder of the cortex do not resemble any structures occurring in a normal gonad. They are, however, almost identical with the tubules in the medulla, and are similar to those in many descended (Baker(2)) and undescended testes of sex intergrade pigs. This similarity, despite the absence of spermatogenesis, appears to warrant calling them spermatic tubules. Their structure and distribution clearly suggest that they have been derived, with comparatively little modification, from cortical or Pfliigerian cords which had not differentiated into definitely ovarian structures. Such an explanation is supported by their persistent superficial attachment, which resembles that of the cortical cords before they have become detached from the embryonic germinal epithelium. The pores by which they open to the exterior possibly represent the persistent remains of the cavities of the hollow invaginations of the germinal epithelium which constituted these cords or tubes of Pfliiger. It is, however, impossible to deny that these pores may have been formed by a secondary perforation or erosion of overlying tissue, in which case they would not be comparable to the original cavities of the cortical cords.


This hypothesis also serves to explain the intermediate stages hetween tubules and follicles which occur in the transition zone between the ovarian and spermatic portions of the cortex. Oocytes occur in this zone in normal follicles, in tubules and in enlarged follicles which are intermediate in character. Apparently the cords in this region developed oocytes but did not differentiate completely into follicles, as in the ovarian region. Consequently some of the oocytes remained in tubules and others became included in normal follicles or abnormal ones of intermediate character. This explanation emphasises the fundamental homology between spermatic tubules and ovarian follicles, and accounts for the close approximation in appearance between sterile spermatic tubules and anovular follicles. The structure of the oocytes in these tubules is not obviously degenerate and does not admit of their dismissal as products of colloidal degeneration (Crew and Fell (7).


The spacial relations of the ovarian and testicular tissue in ovotestes of pigs are constant in all cases described, irrespective of the relative development of the two parts. Baker (3) describes this accurately in stating that the ovarian tissue is situated on the ventro-antero-median surface of the testis, and remarks that ‘‘apparently the corresponding part (whichever that may be) of the embryonic gonad gives rise to ovarian tissue more readily than the remainder.” It is extraordinarily difficult to identify the true morphological position of these parts since the gonad undergoes unequal growth and rotation in relation to the adjacent structures during development. It is, however, known that the anterior end of the embryonic gonad exhibits a more advanced stage of development than the posterior and that the cortex is more developed ventrally than laterally. It would be reasonable, therefore, to suppose that the anteroventral surface of the embryonic gonad would give rise to the ovarian part of the ovotestis.

It is remarkable that a definite epithelium, while present over the ovarian portion, is absent from the spermatic regions of the gonads described. Moreover, the latter have a distinct, although thin, tunica albuginea covering them. Evidently the retention of the germinal epithelium and the development of the tunica albuginea are effected in direct response to the immediately underlying tissues. An exactly similar arrangement has been described in the ovotestis of a pigeon in process of sex-reversal (Brambell and Marrian(5)). The tunica albuginea surrounding the spermatic portions of the cortex is homologous, presumably, to the secondary tunica of the embryonic ovary which persists in‘the normal female.

The sterile condition of the spermatic tubules of these gonads requires mention. This condition is commonly found in undescended testes but Baker (2) has described it also in the descended testes of sex-intergrade pigs. It is probable, therefore, as has been suggested by Crew ®), that this condition does not merely result from non-descent.

Developmental origin

Crew (8) has made an elaborate attempt at explaining hermaphrodite and intersexual pigs by means of a modification of Goldschmidt’s theory of Lymantria intersexes. It is unnecessary to discuss his hypotheses in detail, but the fundamental conception of a time factor, involved in the appearance of the stimuli effecting differentiation of sex, has a special application in the present case. While acknowledging the origin of this conception the author is responsible for its application in this particular case.


At the time when sexual differentiation normally takes place the embryonic gonad consists of the medullary cords surrounded by the primitive tunica albuginea and the germinal epithelium. The testes differentiate positively before the ovaries, the medullary cords transforming into the spermatic tubules, the primitive into the definitive tunica albuginea, and the germinal epithelium degenerating. The ovaries, which are at first distinguishable only by comparison with testes of the same age, soon exhibit a renewed activity of the germinal epithelium resulting in the proliferation of the cortical or Pfligerian cords. The growth of the cortical cords soon results in the disruption of the primitive tunica albuginea and the compression and partial degeneration of the medullary cords in the centre. It is probable that, in some mammals at least, a third proliferation takes place in the differentiated ovary shortly before puberty (de Winiwarter and Sainmont (10)). It is therefore necessary to assume that in a male the stimulus determining the differentiation of the testes is effective almost immediately after the completion of the medullary proliferation. Delay in the appearance of this stimulus would presumably result in the formation of the cortical cords in a peripheral zone around the gonad. These cords always exhibit more advanced development anteriorly and ventrally than posteriorly and laterally. A stage would then be reached when the cortical cords at the antero-ventral end of the gonad had partially disrupted the primitive tunica albuginea and had definitely differentiated into ovarian tissue. The remainder of the cortical proliferation would not have differentiated and would still be outside the primitive tunica albuginea. If it is assumed that the delayed male stimulus became operative at this time, it would be expected to transform the medullary cords and indifferent cortical cords into spermatic tubules and to cause the remains of the primitive tunica albuginea to persist, while having no effect on the already differentiated ovarian tissue. It would also account for the intermediate character of the narrow zone containing oocytes in tubules, and for the invariable occurrence of the ovarian tissue at one pole of the testis and divided from it by a more or less intact tunica albuginea. It is interesting that a stage resembling this condition actually occurs normally in the male mouse embryo, but is transient. Immediately after the testes have differentiated, the germinal epithelium proliferates and forms a thin zone outside the primitive tunica albuginea (Brambell (6)), which is homologous with the cortical proliferation of the ovary. This incipient cortex soon ceases to develop and disappears without ever differentiating at all. The condition, though transient, is comparable to the hypothetical stage required to explain hermaphroditism in the pig.


It is remarkable that in the pig ovotestes the ovarian portion usually contains oocytes and is comparatively normal, whereas the spermatic tubules are invariably sterile and show no indications of spermatogenesis. Apart from this phenomenon the two tissues are mutually compatible and appear to remain permanent constituents of the gonads.


The present example had an ovotestis on one side and a testis on the other. Other cases have been described with two ovotestes, an ovotestis on one side and an ovary on the other, and with an ovary on one side and a testis on the other. Baker (3) has attempted to show a greater tendency of the left side to form an ovary or ovotestis, and of the right a testis or ovotestis. The number of cases recorded are, however, insufficient to warrant any conclusion. The hypothesis advanced in this paper would appear to require a slight variation in the time of development of the gonads on the two sides to account for those cases in which the two gonads differ in their constitution.

Accessory organs

The presence of both ovarian and testicular tissue seems to account sufficiently for the intersexual character of the accessory organs in hermaphrodite pigs, since the development of these organs is controlled by hormones from the gonads. Crew(8) states that hermaphrodite pigs with an ovary on one side develop the epididymis and vas deferens on the other side only, whether this gonad is a testis or ovotestis. He points out that this indicates that the epididymis and vas deferens require some direct stimulus, not a hormonal stimulation alone.


Genetic origin The fact that certain strains of pigs are much more prone to hermaphroditism and intersexuality has been observed a number of times (Baker @, 4), Crew 8), etc.). This suggests, as Crew has pointed out, that genetic factors are involved in their production.

IV. Summary

  1. The reproductive organs of an hermaphrodite pig are described. The right gonad was an ovotestis and the left was a testis. Both gonads consisted of a medulla of spermatic tissue surrounded by a well-developed tunica albuginea and, outside this, a cortical zone of spermatic tubules. The ovarian tissue composed a small part of the cortical zone of the right gonad.
  2. The spermatic tubules of both cortex and medulla were sterile. Those of the cortex opened by distinct pores on the surface of the gonads. Interstitial tissue was plentiful. ,
  3. The ovarian tissue was normal and contained numerous small oocytes in primordial follicles. The region of the cortex between the spermatic and ovarian regions was intermediate in character. Many of the tubules in this region contained true oocytes.
  4. The ovarian tissue was covered on the outside by a cubical epithelium which was absent from the spermatic regions of the cortex, its place being taken by a thin secondary tunica albuginea.
  5. The structure of these gonads can easily be explained embryologically by postulating a slight delay in the appearance of the male determining stimulus.


References

(1) Baxer, J. R. (1925). Brit. Journ. Exp. Biol. vol. 1.

(2) (1925). Q.J.M.S. vol. Lxrx.

(3) —— (1926). Journ. Anat. vol. Lx.

(4) —— (1928). Brit. Journ. Exp. Biol. vol. v1.

(5) BramBeELt, F. W. R. and Marriay, G. F. (1929). Roy. Soc. Proc. B, vol. civ.

(6) BramBett, F. W. R. (1927). Roy. Soc. Proc. B, vol. ct.

(7) Crew, F. A. E. and Fett, H. B. (1922). Q.J.M.S. vol. Lxv1.

(8) Crew, F. A. E. (1924). Journ. Obst. and Gynae. vol. xxxt.

(9) Prox, L. (1914). Arch. f. Mikr. Anat. vol. Lxxxtv.

(10) pE Wintwarter, H. and Satnmont, G. (1909). Arch. de Biol. vol. xx1v.

Plates

DESCRIPTION OF PLATES I, II

GuIpE LETTERS

BV. Blood vessel. GH. Germinal epithelium. IC. Intermediate zone of cortex. I7'. Interstitial tissue. M. Medulla. O. Oocytes. OT. Oocytes in tubules. OV. Ovarian zone of cortex. P. Peritoneal pore of cortical spermatic tubule. S. Ovarian stroma. SC. Spermatic zone of cortex. ST. Spermatic tubule. 7,. Primary tunica albuginea. T,. Secondary tunica albuginea. VD. Vas deferens.

Plate I

Figs. 1 and 2. Dorsal and ventral aspects of the organs described. The upper gonad is the right and the lower the left in both figs. nat. size.

Fig. 3. Section of portion of left epididymis. x 27.

Fig. 4. Section of medial uterus showing well-developed uterine mucosa with glands and the two vasa deferentia in the broad ligament. x 14.

Plate II

Fig. 1. Ovarian region of cortex, showing germinal epithelium and oocytes in primordial follicles embedded in typical stroma. x 100.

Fig. 2. Spermatic region of cortex, showing tubules opening to the surface, interstitial cells and the thick primary and very thin secondary tunica albuginea. x 100.

Fig. 3. Intermediate zone of cortex, showing oocytes in tubules and one in a primordial follicle. The ovarian nature of the stroma and the interstitial cells are also shown. x 100.

Fig. 4. Ovotestis, showing ovarian, intermediate, and testicular regions of cortex, and the primary tunica albuginea surrounding the medulla and including in it one large lobule of spermatic tissue. x 20.

Fig. 5. Medullary region of ovotestis, showing spermatic tubules and interstitial tissue. x 100.


The author is indebted to Mr D. A. Kempson for the photographs reproduced in Plate I, figs. 1 and 2, and to Mr F, J. Pittock for the photomicrographs.



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