Book - Comparative Embryology of the Vertebrates 1-1

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

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Part I The Period of Preparation

Part I - The Period of Preparation: 1. The Testis and Its Relation to Reproduction | 2. The Vertebrate Ovary and Its Relation to Reproduction | 3. The Development of the Gametes or Sex Cells

The Testis and Its Relation to Reproduction

A. Introduction

1. General Description of the Male Reproductive System

The male reproductive system of most vertebrate animals consists of two testis with a sperm-conveying duct and attendant auxiliary glands associated with each testis. In some species, such as the frog and many teleost fishes, the sperm-conveying duct is a simple structure, but in most vertebrate forms there is a tendency for the duct to be complicated. The cyclostomatous fishes do not possess sperm-conveying ducts from the testis to the outside.

In reptiles, some birds and all mammals, in gymnophionan amphibia and in the “tailed” frog, Ascaphus, in sharks and certain teleost fishes, an intromittent organ is added to the sperm-conveying structures for the purpose of internal fertilization. But an intromittcnt organ is not present in all species which practice internal fertilization. In many salamanders, internal fertilization is effected by the spawning of a spermatophore filled with sperm; the latter is picked up by the cloaca of the female. The sperm in these salamanders are stored in special pockets or tubules within the dorsal wall of the cloaca. These storage tubules form the spermatheca (fig. 10). Direct transfer of sperm to the female by cloacal contact may occur in some species.

2. Importance of the Testis

The word testis or testicle was formerly applied to the ovary of the female, as well as to the male sperm-producing organ, and the term "female testicle" was used in reference to the female organ. The use of the word “ovary” was introduced by Steno in 1667, and also by de Graaf (fig. 1 ) in 1672 in his work on the female generative organs. To quote from de Graaf: “Thus, the general function of the female testicles is to generate the ova, to nourish them, and to bring them to maturity, so that they serve the same purpose in women as the ovaries of birds. Hence, they should rather be called ovaries than testes because they show no similarity, either in form or contents, with the male testes properly so called.” (See Corner, -43.) From the time of de Graaf the word “testis” has been restricted to designate the male organ essential to reproduction.

The phrase "essential to reproduction" does not describe fully the importance of testicular function. As we shall see later on, the testis not only assumes the major role in the male's activities during the period of reproduction, but also, in the interim between specific reproductive periods, it governs in many instances male behavior leading to protection and preservation of the species. Thus, the testis is the organ responsible for maleness in its broader, more vigorous sense.

B. Anatomical Features of the Male Reproductive System

Before endeavoring to understand the general functions of the testis in relation to reproduction, it is best to review some of the structural relationships of the testis in the vertebrate group.

Fig. 1. Reinier de Graaf. Born in Holland, 1641; died in Delft, Holland, 1673. Author of important works on the generative organs of the female. Described the Graafian follicle in the ovary of mammals but erroneously believed it to be the mammalian egg. (From Corner, '43.)

1. Anatomical Location of the Testis

In most vertebrates other than mammals, the testes are suspended well forward within the peritoix eal^cayity. In the Mammalia, however, the condition is variable. In the monotrematous mammals. Echidna and Ornithorynchus, the testes are located within the peritoneal cavity near the kidneys. In the elephant the testes also are located in this area. Schulte (’37) describes the position of the testes in an Indian elephant (Elephas indicus), 20 years old, as being “retroperitoneal lying on each side medial to the lower pole of the kidney.” (The kidneys were found to lie retroperitoneally on either side of the lower thoracic and lumbar vertebrae, and each measured about 275 mm. in length.) However, in the majority of mammals the testes descend posteriad from the original embryonic site, the extent varying with the species. In some there is a slight posterior migration, and the testes of the adult are situated well forward in the pelvic region. Examples of this condition are found in conies, whales, sea cows, African jumping shrews, and in armadillos. In sloths and American anteaters, the testes may descend into the pelvic cavity and lie in the area between the urinary bladder and the posterior body wall. However, in most of the eutherian and marsupial mammals, a dual outpushing of the postero-ventral body wall occurs into which the testes come to lie either permanently, or, in some forms, temporarily during the breeding season. This outward extension of the body-wall tissues is known as the scrotum; it involves not only the skin, muscle and connective tissues of the body wall but the peritoneal lining as well (fig. 2). (The interested student may consult Weber (’28) and Wislocki (’33) for data concerning the extent of testis descent in mammals.)

The peritoneal evaginations into the scrotal sac are two in number, one for each testis; each evagination is known as a processus vaginalis (figs. 3E, F; 4A, B). In many mammals this evagination becomes separated entirely froln the peritoneal cavity, and the testis, together with a portion of the sperm-conveying duct, lies suspended permanently in a small antechamber known as the inguinal bursa or serous cavity of the scrotum (fig. 4B). (See Mitchell, ’39.) This condition is found in the horse, man, opossum, bull, ram, dog, cat, etc. In certain other mammals, such as the rat, guinea pig, and ground hog, the inguinal bursa does not become separated from the main peritoneal cavity, and a persistent inguinal canal remains to connect the inguinal bursa with the peritoneal cavity (fig. 4C). In some rodents the testes pass through this persisting inguinal canal into the scrotum as the breeding season approaches, to be withdrawn again after the breeding period is terminated. The ground squirrel, Citellus tridecemlineatus (Wells, ’35) and the ground hog, Marrnota monax (Rasmussen, ’17) are examples of mammals which experience a seasonal descent of the testis.

In the majority of those mammals possessing a scrotum, it is a permanent structure. In a few, however, it is a temporary affair associated with the breeding season, as in the bat, Myotis, where the testes pass into a temporary perineal pouch or outpushing of the posterior abdominal wall during the reproductive season, to be withdrawn again together with the scrotal wall when the breeding period is past (fig. 4D). A similar periodic behavior is true of many insectivores, such as the common shrews, the moles, and the European hedgehog (Marshall, ’ll).

Fig. 2. Sketch of male reproductive system in man.

The permanent scrotum is a pendent structure, in some species more so than others. In the bull and ram, it extends from the body for a considerable distance, whereas in the cat, hippopotamus, tapir, guinea pig, etc., it is closely applied to the integumentary wall. In primates, including man, in most carnivores, and many marsupials, the pendency of the scrotum is intermediate between the extremes mentioned above.

An exceptional anatomical position of the testes in the lower vertebrates is found in the flatfishes, such as the sole and flounder, where they lie in a caudal outpouching of the peritoneal cavity (fig. 5). The testis on either side may even lie within a special compartment in the tail. (The ovaries assume the latter position in the female.)

Fig. 3. Diagrammatic representations of the urogenital structures in the developing male pig, with special emphasis upon testicular descent. (A) Early relationship of the genital fold (genital ridge), mesonephric kidney and its duct, together with the metanephric kidney and the ureter in 20-mm. pig embryo. The relationship of the mesonephric and metanephric ducts to the urogenital sinus is shown. The Miillcrian duct is omitted. (B) Male pig embryo about 45-mm., crown-rump length, showing relationship of gonad and metanephric kidney. I he metanephric kidney is shown below (dorsal to) the mesonephric kidney. The gonad (testis) is now a well-defined unit. The portion of the genital fold tissue anterior to the testis becomes the anterior suspensory ligament of the testis, while the genital fold tissue caudal to the testis continues back to join the inguinal ligament of the mesonephros (the future gubernaculum). (C) About 80-mm., crown-rump, pig embryo. Observe that the metanephros is now the dominant urinary organ and has grown cephalad, displacing the mesonephric kidney which is regressing and moving caudally with the testis. The remains of the mesonephric kidney at this time are gradually being transformed into epididymal structures. (D) About 130~mm.. crown-rump, pig embryo. Observe that the testis is approaching the internal opening of the inguinal canal. The anterior suspensory ligament is now an elongated structure extending over the lateroventral aspect of the metanephric kidney; the gubernacular tissue is shown extending downward into the inguinal canal. (E) Later stage in testicular descent. The anterior suspensory ligament of the testis is a prominent structure, while the gubernaculum is compact and shortened. (F) The condition found in the full-term, fetal pig. The testis is situated in the scrotal swelling; the gubernaculum is much shortened, while the anterior suspensory ligament remains as a prominent structure, extending cephalad to the caudal portions of the metanephric kidney.

2. Possible Factors Involved in Testis Descent The descent of the testis within the peritoneal cavity and into the scrotum poses an interesting problem. In embryonic development extensive migration of cell substance, or of cells, tissues, and organ structures is one of many processes by which the embryonic body is formed. That is to say, the dynamic movement or displacement of developing body structures from their original position is a part of the pattern of development itself. The casual factors involved in such movements are still unknown, and the study of such behavior forms one of the many interesting aspects of embryological investigation awaiting solution.

Fig. 4. Diagrammatic drawings portraying the relationship of the testis to the processus vaginalis (peritoneal evagination) and the scrotum. The testis is at all times retroperitoneal, i.e., outside the peritoneal cavity and membrane. (A) Earlier stage of testicular descent at the time the testis is moving downward into the scrotum. (B) Position of the testis at the end of its scrotal journey in a form possessing permanent descent of the testis, e.g., man, dog, etc. (C) Testis-peritoneal relationship in a form which does not have a permanent descent of the testis — the testis is withdrawn into the peritoneal cavity at the termination of each breeding season. Shortly before the onset of the breeding period or “rut,” the testis once again descends into the scrotum, e.g., ground hog. (D) Position of testis in relation to body wall and peritoneum in the mole, shrev/, and hedgehog in which there is no true scrotum. The testis bulges outward, pushing the body wall before it during the breeding season. As the testis shrinks following the season of rut, the bulge in the body wall recedes. True also of bat, Myotis.

Fig. 5. Opened peritoneal cavity of a common flounder, Limanda ferruginea, showing the position occupied by the testes. Each testis is situated partly in a separate compartment on either side of the hemal processes of the tail vertebrae.

Various theoretical explanations have been proposed, however, to explain the movement of the testis posteriad from its original embryonic site. Classical theory mentions the mechanical pull or tightening stress of the gubernaculum, a structure which develops in relation to the primitive genital fold or genital ridge (figs. 3B, C; 351C-7).

The genital ridge extends along the mesial aspect of the early developing mesonephric kidney from a point just caudal to the heart to the posterior extremity of the mesonephric kidney near the developing cloacal structures (Hill, ’07). Anteriorly, the genital ridge (fold) merges with the diaphragmatic ligament of the mesonephros (fig. 3A). The gonad (testis or ovary) develops in a specialized region of the more cephalic portion of the genital ridge (Allen, ’04). (See fig. 3A.) The caudal end of the mesonephric kidney eventually becomes attached to the posterior ventral body wall by means of a secondary formation of another cord of tissue, the inguinal fold (fig. 3A). The latter is attached to the posterior ventral body wall near the area where the scrotal outpushing (evagination) later occurs. This inguinal fold later becomes continuous with the genital fold (fig. 3B). The inguinal fold thus becomes converted into a ligament, the inguinal ligament of the mesonephros, uniting the caudal portion of the mesonephric kidney and adjacent genital fold tissue with the area of scrotal evagination (fig. 3B). The gubernaculum represents a later musculo-connective tissue development of the inguinal ligament and the adjacent genital fold tissue. It contains smooth muscle fibers as well as connective tissue. As the scrotal evagination forms at the point where the gubernaculum attaches to the body wall, the gubernaculum from the beginning of its formation is connected with the developing scrotal sac.

As the testis migrates posteriad, the anterior suspensory ligament of the testis elongates and the gubernaculum shortens (fig. 3A~F). This decrease in length of the gubernaculum is both real and relative. It is real in that an actual shortening occurs; it is relative because the rapid enlargement of the developing pelvic cavity and its contained organs makes the length of the gubernaculum appear less extensive. This enlargement of the pelvic space and increase in size of its contained structures and a corresponding failure of the gubernaculum to elongate, certainly are factors in bringing about the intra-abdominal descent of the testis; that is, testis descent within the peritoneal cavity itself (Felix, '12).

Developmental preparations precede the extra-abdominal descent of the testes, for the scrotal chambers must be prepared in advance of the arrival of the testes. These developmental events are:

(1) two outpocketings of the abdominal wall which come to lie side by side below the skin to form the walls of the scrotal chamber, and

(2) an evagination of the peritoneum into each of the abdominal outpocketings which act as peritoneal linings for each pocket.

It is worthy of mention that the above outpushings of the abdominal wall and of the peritoneum precede the movement of the testes into the scrotum. They serve to illustrate the theory that a shortening of the gubernaculum is not sufficient to explain testis descent. Rather, that in this descent a whole series of developmental transformations are involved; the shortening of the gubernaculum and scrotal development merely represent isolated phases of the general pattern of movement and growth, associated with this descent.

More recent research emphasizes the importance of certain physiological factors relative to the descent problem. It has been determined, for example, that administration of the gonadotrophic hormone of pregnancy urine (chorionic gonadotrophin) or of the male sex hormone, testosterone, aid the process of extra-abdominal descent (i.c., descent from the inguinal ring area downward into the scrotum) . Hormone therapy, using chorionic gonadotrophin together with surgery, is used most often in human cryptorchid conditions. The androgen, testosterone, aids testicular descent mainly by stimulating the growth of the scrotal tissues and the vas deferens; however, it is not too successful in effecting the actual descent of the testis (Robson, '40; Wells, '3; Pincus and Thimann, '50).

The phenomenon of testicular migration thus is an unsolved problem. Many activities and factors probably play a part in ushering the testis along the pathway to its scrotal residence.

3. General Structure of the Scrotum and the Testis in Mammals

a. Structure of the Scrotum

The scrotal modification of the body wall generally occurs in the posteroventral area between the anus and the penial organ. However, in marsupials it is found some distance anterior to the latter.

Each scrotal evagination consists of three general parts: the skin with certain attendant muscles, the structures of the body wall below the skin, and the peritoneal evagination. The skin, with its underlying tunica daitos muscle tissue and superficial perineal fascia, forms the outer wall of the scrotum (fig. 6). Within this outer cutaneous covering lie the two body-wall and two peritoneal evaginations. The body-wall evaginations involve connective and muscle tissues of the external oblique, internal oblique, and trans versus muscles. The caudal part of each peritoneal outpocketing forms the serous cavity or inguinal bursa in which the testis is suspended after its descent, and its more anterior portion forms the inguinal canal (figs. 2, 4B, 6). The oblique and transversus layers of tissues thus are molded into a musculo-connective tissue compartment around each serous cavity. The median septum of the scrotum represents the area of partial fusion between the two musculo-connective tissue compartments, whereas the median raphe of the scrotum denotes the area of fusion of the two cutaneous coverings of the body-wall outpushings (fig. 6).

Consequently, passing inward from the superficial perineal fascia of the skin or outer wall, one finds the following tissue layers surrounding the testis:

1. The external spermatic fascia represents the modified fascia of the external oblique muscle layer of the embryo.
2. The middle spermatic fascia is a modification of the internal oblique muscular layer, whose tissue forms the cremaster muscle loops within the scrotum (fig. 6). (Some of the cremasteric musculature may be derived from the transversus layer.)
3. The internal spermatic fascia or tunica vaginalis communis is derived from the transverse muscle layer of the embryo.
4. Along the inner surface of the tunica vaginalis communis is the peritoneal membrane. The latter is reflected back over the surface of the suspended testis, and thus forms the visceral peritoneal covering of the testis. This lining tissue of the common vaginal tunic and the peritoneal membrane which covers the testis are derived from the original peritoneal evagination into the scrotal pocket; as such it forms the tunica vaginalis propria*

b. General Structure of the Testis

The testis is composed of the following structural parts:

(1) The inner layer of the tunica vaginalis propria, the tunica vaginalis internus, envelops the testis. The cavity between the outer and inner layers of the tunica vaginalis propria is the inguinal bursa. Obliteration by injury or infection of this inguinal bursa may cause degenerative changes in the testis. In other words, the testis normally must be free to move within its serous (peritoneal) cavity.

(2) Within the tunica vaginalis internus of the testis is a thick fibrous layer of connective tissue, the tunica albuginea (fig. 7). From this tunic, connective tissue partitions, the septula of the testis, extend inward and converge toward that testicular zone where supplying blood vessels enter and leave, including the lymphatics. The latter zone is known as the mediastinum testis and it represents a regional thickening of the tunica albuginea. Here the connective tissue fibers form a latticework which acts as a framework for the larger blood and lymph vessels and efferent ducts of the testis. The testis is attached to the scrotal wall in the mediastinal area.

(3) The spaces between the various septula partitions form the septula compartments. In the human testis there are about 250 septula compartments, each containing a lobule of the testis. The lobuli testis contain the convoluted portions of the seminiferous tubules. From one to three seminiferous tubules are found in each lobule; they may anastomose at their distal ends. The combined length of all the seminiferous tubules approaches 250 meters in the human. The convoluted portions of the seminiferous tubules empty into the straight tubules (tubuli recti) and these in turn unite with the rete tubules located within the substance of the mediastinum. Connecting with the rete tubules of the testis, there are, in man, from 12 to 14 ductuli efferentes (efferent ductules of the epididymis) of about 4 to 6 cm. in length which emerge from the mediastinum and pass outward to unite with the duct of the epididymis. The epididymal duct represents the proximal portion of the reproductive duct which conveys the male gametes to the exterior.

Fig. 6. Schematic drawing of the testis and its relationship within the scrotum. On the right side of the drawing the muscle and connective-tissue layers surrounding the inguinal bursa and testis are shown; on the left side may be seen the loops of the cremaster muscle surrounding the tunica vaginalis communis.

Fig. 7. Diagrammatic representation of the general structural relationship of the parts of the human testis. (Modified from Corner, 1943, after Spalteholz and Huber.)

4. Specific Structures of the Mammalian Testis Which Produce THE Reproductive Cells and the Male Sex Hormone

Two very essential processes involved in reproduction are the formation of the sex cells or gametes and the elaboration of certain humoral substances, known as sex hormones. Therefore, consideration will be given next to those portions of the testis which produce the sperm cells and the male sex hormone, namely, the seminiferous tubules and the interstitial tissue.

a. Seminiferous Tubules

The seminiferous tubules lie in the septula compartments (fig. 7). The word seminiferous is derived from two Latin words: semen, denoting seed, and ferre, which means to bear or to carry. The seminiferous tubule, therefore, is a male “seed-bearing” structure. Within this tubule the male gametes or sperm are formed, at least morphologically. However, the word semen has a broader implication in that it is used generally to denote the entire reproductive fluid or seminal fluid. The seminal fluid is a composite of substances contributed by the seminiferous tubules and various parts of the accessory reproductive tract.

The exact form and relationship of the various seminiferous tubules (tubuli seminiferi) which occupy each testicular compartment have been the object of much study. It is a generally accepted belief at present that the tubules within each testicular lobule are attached at their distal ends; that is, that they anastomose (fig. 7). Some investigators also believe that there may be other anastomoses along the lengths of these very much contorted and twisted structures. Moreover, it appears that the septula or testicular compartmental partitions are not always complete; the seminiferous tubules of one lobule thus have the opportunity to communicate with those of adjacent lobules. The seminiferous tubules of any one lobule join at their proximal ends and empty into a single straight seminiferous tubule. The straight tubules or tubuli recti pass into the mediastinum and join the anastomosing rete tubules of the rete testis.

The convoluted portions of the seminiferous tubules produce the sperm (spermia; spermatozoa). In the human testis, the length of one of these tubules is about 30 to 70 cm. and approximately 150 /a to 250 ix in diameter. Each tubule is circumscribed by a basement membrane of connective tissue and contains two cell types:

( 1 ) supporting or Sertoli cells, and

(2) spermatogenic cells or spermatogonia (see fig. 8 and Chap. 3).

The cells of Sertoli are relatively long, slender elements placed perpendicularly to the basement membrane to which they firmly adhere. These cells may undergo considerable change in shape, and some observers believe that they may form a syncytium, known as the “Sertolian syncytium.” Others believe them to be distinct elements. It is said that Sertoli cells may round up and form phagocytes which become free from the basement membrane and move, ameba-like, in the lumen of the seminiferous tubule, phagocytizing degenerating sperm cells. However, their main function appears to be associated with the development of sperm during the period when the latter undergo their transformation from the spermatid condition into the adult

Fig. 8. Semidiagram matic representation of section of cat testis, showing seminiferous tubules and interstitial tissue, particularly the cells of Leydig.

Sperm form. The Sertolian cells thus may act as nursing elements during sperm metamorphosis.

The spermatogenic cells or spermatogonia (germinal epithelium of the tubule) lie toward the outer portion of the seminiferous tubule between the various Sertoli elements. As a rule spermatogonia lie apposed against the basement membrane of the tubule (see fig. 8 and Chap. 3).

b. Interstitial Tissue

The interstitial tissue of the testis is situated between the seminiferous tubules (fig. 8). It consists of a layer of connective tissue applied to the basement membrane of the seminiferous tubule and of many other structures, such as small blood and lymph vessels, connective tissue fibers, connective tissue cells, mast cells, fixed macrophages, etc. The conspicuous elements of this tissue are the so-called interstitial cells or cells of Leydig (fig. 8). In man, cat, dog, etc., the cells of Leydig are relatively large, polyhedral elements, possessing a granular cytoplasm and a large nucleus.

5. The Testis of Vertebrates in General

In the vertebrate group, the testis shows marked variations in shape and size. In many fishes, the testes are irregular, lobular structures, but in other fishes, amphibia, reptiles, birds, and mammals, they assume an ovoid shape. The size of the testis is extremely variable, even in the same species. The testis of the human adult approximates 4 to 5 cm. in length by 3 cm. wide and weighs about 14 to 19 Gm. The testis of the horse averages 11 cm. long by 7 cm. wide with a weight of 30 to 35 Gm., while that of the cat is 1.6 cm. long and 1.1 cm. wide with a weight of 1.5 Gm. In the mud puppy, Necturus, the testis is approximately 3.5 cm. long and 0.8 cm. wide with a weight of 0.3 Gm. The testis of the large bullfrog is 1 .2 cm. by 0.5 cm. with a weight of 0.8 Gm. In comparison to the foregoing, Schulte (’37) gives the weight of each testis of an Indian elephant as two kilograms!

Regardless of size or shape, the presence of seminiferous tubules and interstitial tissue may be observed in all vertebrate testes. In some species the seminiferous tubule is long; in others it is a short, blunt affair. The interstitial cells may be similar to those described above, or they may be small, inconspicuous oval elements.

6. Accessory Reproductive Structures of the Male a. The Reproductive Duct in Forms Utilizing External Fertilization

The accessory reproductive organs of the vertebrate male are extremely variable in the group as a whole. A relatively simple reproductive duct (or in some no duct at all) is the rule for those forms where fertilization is effected in the external medium. In cyclostome fishes, for example, the reproductive cells are shed into the peritoneal cavity and pass posteriad to emerge externally by means of two abdominal pores. Each pore empties into the urogenital sinus. In teleost fishes (perch, flounder, etc.) the conveying reproductive duct is a short, simple tube continuous with the testis at its caudal end and passing posteriorly to the urogenital sinus (fig. 9A). In frogs and toads, as well as in certain other fishes, such as Amia and Polypterus, the male reproductive duct is a simple, elongated tube associated with the testis by means of the efferent ductules of the latter, coursing posteriad to open into the cloaca (frogs and toads) or to the urogenital sinus (Amia; Polypterus) (fig. 9B, C). Simplicity of sperm duct development and external union of the gametes are associated reproductive phenomena in the vertebrate group.

b. The Reproductive Duct in Species Practicing Internal Fertilization

An entirely different, more complex male reproductive duct is found (with some exceptions) in those vertebrates where gametic union occurs within the protective structures of the maternal body. Under these circumstances there may be a tendency for one male to serve several females. Enlargement of the duct with the elaboration of glandular appendages, and structures or areas for sperm storage is the rule under these conditions (fig. 9D--F). This form of the male genital tract is found not only in those species where an intromittent organ deposits the sperm within the female tract, but also where the sperm are deposited externally in the form of spermatophores (fig. 10).

In many species, the reproductive duct is greatly lengthened and becomes a tortuous affair, especially at its anterior or testicular end. In fact, the cephalic end of the duct may be twisted and increased to a length many times longer than the male body itself. This coiled, cephalic portion is called the duct of the epididymis (epididymides, plural). (See figs. 7, 9E.) The word epididymis is derived from two Greek words: epi = upon, and didymis = testicle. The epididymis, therefore, is the body composed of the tortuous epididymal duct and the efferent ducts of the testis which lie upon or are closely associated with the testis. The complex type of reproductive duct is composed thus of two main portions, an anterior, contorted or twisted portion, the epididymal duct, and a less contorted posterior part, the vas deferens or sperm duct proper (fig. 9D, E).

In some vertebrates, in addition to the above complications, the caudal end of the reproductive duct has a pronounced swelling or diverticulum, the seminal vesicle (e.g., certain sharks and certain birds). The latter structures are true seminal vesicles in that they store sperm during the reproductive period.

The epididymal duct in man is a complex, coiled canal composed of a head (caput), a body (corpus), and a tail (cauda). (See fig. 7.) It is C-shaped with its concavity fitting around the dorsal border of the testis, the head portion being located at the anterior end of the latter. The total length of the epididymal duct in man is said to be about 4 to 7 m. In other mammals the epididymal duct may be much longer. For example, in the ram, from 40 to 60 m.; in the boar, 62 to 64 m.; in the stallion, 72 to 86 m. (Asdell, ’46). At its caudal end it becomes much less tortuous and gradually passes into the vas deferens (ductus deferens).

Fig. 9. Various vertebrate testes and reproductive ducts, emphasizing the relative simplicity of the duct where external fertilization is the rule while complexity of the duct is present when internal fertilization is utilized. There are exceptions to this rule, however. (A) Flounder (Limanda ferruginea). (B) Frog (Rana catesbiana). (C) Urodele (Cryptobranchus alleganiensis). (D) Dog shark (Squalus acanthias), (E) Urodele (Necturus rnaculosus). (F) Rooster (G alius domestic us).

The ductus deferens has a length of about 30 to 35 cm. in man. Leaving the scrotum it passes anteriad together with accompanying nerves and blood vessels in the subcutaneous tissue over the front of the pelvic bone into the peritoneal cavity through the inguinal ring (fig. 2). Here it separates from the other constituents of the spermatic cord (i.e., it separates from the nerves and blood vessels) and passes close to the dorsal aspect of the bladder and dorsally to the ureter. It then turns posteriad along the dorsal aspect of the neck of the bladder and the medial region of the ureter, and accompanied by its fellow duct from the other side, it travels toward the prostate gland and the urethra. Just before it enters into the substance of the prostate, it receives the duct of the seminal vesicle. The segment of the vas deferens from the ureter to the seminal vesicle is considerably enlarged and is called the ampulla. After receiving the duct of the seminal vesicle, the vas deferens becomes straightened and highly muscularized — as such it is known as the ejaculatory duct. The latter pierces the prostate gland located at the caudal end of the bladder and enters the prostatic portion of the urethra; from this point the urethra conveys the genital products.

The auxiliary glands associated with the genital ducts of the human male consist of the seminal vesicles, the prostate gland, Cowper’s glands, and the glands of Littre.

The seminal vesicles are hollow, somewhat tortuous bodies (fig. 2). Each vesicle arises in the embryo as an outpushing (evagination) of the vas deferens. The prostate gland has numerous excretory ducts which empty into the urethra. It represents a modification of the lining tissue of the urethra near the urinary bladder together with surrounding muscle and connective tissues. Cowper’s (bulbourethral) glands are small pea-shaped structures placed at the base of the penial organ; their ducts empty into the urethra. The glands of Littre are small, glandular outgrowths along the urethra and are closely associated with it.

To summarize the matter relative to the structural conditions of the reproductive duct in the male of those species which practice internal fertilization:

1. A lengthening and twisting of the duct occurs.
2. A sperm-storage structure is present, either as a specialized portion of the duct or as a sac-like extension.
3. Certain auxiliary glands may be present. These glands are sometimes large and vesicular structures, such as the seminal vesicles of the human duct, or they may be small glands distributed along the wall of the duct, such as the glands of Littre.

C. Specific Activities of the Various Parts of the Male Reproductive System

1. Introduction

a. Three General Functions of the Male Reproductive System The activities of the testes and the accessory parts of the male reproductive system result in the performance of three general functions as follows:

1. formation of the semen, # delivery of the semen to the proper place where the sperm may be utilized in the process of fertilization, and # elaboration of the male sex hormone.

b. Some Definitions Semen or seminal fluid is the all-important substance which the male contributes during the reproductive event. It is the product of the entire reproductive system, including special glands of the accessory reproductive structures. The semen is composed of two parts: (1) The sperm (spermatozoa, spermia) are the formed elements which take part in the actual process of fertilization. (2) The seminal plasma, a fluid part, is a lymph-like substance containing various substances dissolved or mixed in it. These contained substances are important as a protection for the sperm and as an aid to the process of fertilization.

With regard to the second function of the male genital system, namely, the delivery of sperm to the site of fertilization, it should be observed that in some vertebrates this is a more simple problem than in others. In those forms which practice external fertilization, the male system simply discharges the seminal fluid into the surrounding external medium. However, in those vertebrates where internal fertilization is the rule, the female system assumes some of the burden in the transport of the semen to the region where fertilization is consummated, thus complicating the procedure. In these instances, the male genital tract is called upon to produce added substances to the seminal fluid which aid in protecting the sperm en route to the fertilization site.

Fig. 10. Spermatophores of common urodeles. (Redrawn from Noble: Biology of the Amphibia, New York, McGraw-Hill.) (A) Triturus viridescens. (After Smith.) (B) Desmognathus fuscus, (After Noble and Weber.) (C) Eiirycea hislineata.

The elaboration of the androgenic or male sex hormone is a most important function. Androgenic or male sex hormone substances are those organic compounds which induce maleness, for they aid the development of the male secondary sex characteristics, enhance the growth and functional development of the male accessory reproductive structures, and stimulate certain aspects of spermatogenesis.' Like the estrogens, androgens are not confined to a particular sex; they have been extracted from the urine of women and other female animals. The androgens derived from urinary concentrates are androsterone and dehydroisoandrosterone. These two androgens are not as powerful as that prepared from testicular tissue. Testicular androgen was first isolated from testicular tissue in 1935 and was given the name testosterone. It also has been synthesized from cholesterol. It is the most powerful of the androgens and probably similar, if not identical, with the substance produced in the testis (Koch, '42).

2. Activities of the Testis

a. Seasonal and N on-seasonal Types of Testicular Activity The testis has two main functions: the production of sperm and formation of the male sex hormone. In many vertebrates these two activities represent a continuous procedure during the reproductive life of the male animal. This condition is found in certain tropical fish, in the common fowl and various wild tropical birds, and in many mammals, such as man, the dog, bull, stallion, cat, etc. On the other hand, in the majority of vertebrates these activities of the testis are a seasonal affair. This condition is found in most fish, practically all amphibia, all temperate -zone-inhabiting reptiles, most birds, and many mammals. Among the latter, for example, are the ferret, deer, elk, fox, wolf, and many rodents, such as the midwestern ground squirrel. Seasonal periodicity is true also of the common goose and turkey.

Fig. 11. Seasonal spermatogenesis and accessory gland development in the ground squirrel, Citellus tridecemlineatus. Stippling below base line shows period of hibernation, whereas crosshatching reveals the reproductive period. (From Turner: General Endocrinology, Philadelphia, Saunders, after L, J. Wells.)

Sperm-producing periodicity is not correlated with any particular season, nor is spermatogenesis always synchronized with the mating urge, which in turn is dependent upon the male sex hormone. In some forms, these two testicular functions may actually occur at different seasons of the year, as for example, in the three-spined stickleback, Gasterosteus aculeatus (fig. 15). (See Craig-Bennett, '31.) In general, it may be stated that sperm are produced during the weeks or months which precede the development of the mating instinct. Many species follow this rule. For example, in the bat of the genus Myotis, sperm are produced during the late spring and summer months, while mating or copulation takes place during the fall or possibly early the next spring (Guthrie, '33). In the common newt, Triturus viridescens, spermatogenesis comes to pass during the warm months of the summer, and sperm are discharged from the testis into the reproductive ducts during the late fall and early spring, while copulation is accomplished in the early spring. The testes in this species are quiescent during the cool winter months. In the midwestern ground squirrel, Citellus tridecemlineatus, spermatogenesis begins in November and is marked during February and March (fig. 11). The animal hibernates away the winter months and emerges the first part of April in a breeding condition. Mating occurs in the early spring (Wells, '35). In the garter snake, Tharnnophis radix, sperm are produced in the testes in the summer months, stored in the epididymides during the hibernation period in the fall and winter, and used for copulation purposes in the spring (Cieslak, '45). Again, in the Virginia deer, Odocoileus virginianus borealis, studied by Wislocki ('43), active spermatogenesis is realized during the summer and early autumn months, while the mating season or “rut” which results from the driving power of the male sex hormone, is at its peak in October and November (fig. 12). In the fox. Bishop ('42) observed spermatogenesis to begin in the late fall months, while mating is an event of the late winter and early spring. In April and May the seminiferous tubules again assume an inactive state (fig. 13). In the common frog, Rana pipiens, spermatogenesis is present in the summer months and morphogenesis of spermatids into sperm happens in large numbers during September, October, and November. Sperm are stored in the testis over the winter, and the mating instinct is awakened in the early spring (Glass and Rugh, '44). Following the mating season in spring and early summer the testis of the teleost, Fundulus heteroclitus, is depleted of sperm until the next winter and spring (Matthews, '38). As the seasonal type of testicular activity is present in a large number of vertebrate species, it seems probable that it represents the more primitive or fundamental type of testicular functioning. b. Testicular Tissue Concerned with Male Sex-hormone Production While one cannot rule out the indirect effects which activities of the seminiferous tubules may have upon the functioning of the testis as a whole, including the interstitial tissue, direct experimental evidence and other observations suggest that the interstitial tissue holds the main responsibility for the secretion of the male sex hormone, testosterone, or a substance very closely allied to it. For example, if a testis from an animal possessing a permanent scrotum is removed from the inguinal bursa and placed within the peritoneal cavity, the seminiferous tubules tend to degenerate, but the interstitial tissue remains. The sex hormone, under these circumstances, continues to be produced. Again, males having cryptorchid testis (i.e., testes which have failed in their passage to the scrotum) possess the secondary sex characteristics of normal males but fail to produce sperm cells. Also, it has been demonstrated that the mammalian fetal testis contains the male sex hormone. However, in this fetal condition, the seminiferous tubules are present only in an undeveloped state, whereas interstitial tissue is well differentiated. It is probable in this case that the interstitial tissue of the fetal testis responds to the luteinizing hormone in the maternal blood.

Fig. 12. Sections of the testis of the deer, Odocoileus virginianus borealis. (After Wislocki.) (A) Seminiferous tubules of deer in June. Observe repressed state of tubules and absence of sperm. (B) Epididymal duct of same deer. Observe absence of sperm and smaller diameter of duct compared with (D). (C) Seminiferous tubules of October deer; spermatogenic activity is marked. (D) Epididymal duct, showing well-developed epididymal tube and presence of many sperm.

In hypophysectomized male rats injected with dosages of pure folliclestimulating hormone (FSH) or with small doses of pure luteinizing hormone (LH; ICSH), the seminiferous tubules of the testis respond and spermatogenesis occurs. However, the interstitial tissue remains relatively unstimulated and the accessory structures continue in the atrophic state. If larger doses of the luteinizing factor are given, the interstitial tissue responds and the secondary sexual characters are developed, showing a relationship between interstitial activity and sex-hormone production. (Consult Evans and Simpson in Pincus and Thimann, '50, pp. 355, 356.) From certain species whose reproductive activities are confined to a particular season of the year, there also comes evidence that the interstitial tissue is the site of sex-hormone production. In the behavior of testicular tissue in the stickleback, Gasterosteus, as shown by van Oordt ('23) and Craig-Bennett ('31) sperm are produced actively in the seminiferous tubules during one period of the year when the interstitial tissue is in an undeveloped condition. The secondary sex characters also are in abeyance at this season of the year. However, during the months immediately following sperm production, sperm are stored within the seminiferous tubules and active spermatogenesis is absent. When the seminiferous tubules thus have completed their spermatogenic activity, the interstitial tissue begins to increase, followed by a development of secondary sex characteristics (figs. 14, 15). A similar difference in the rhythm of development of these two testicular tissues can be shown for many other vertebrates. All of these suggestive facts thus serve to place the responsibility for male sex-hormone production upon the interstitial tissue, probably the cells of Leydig.

Fig. 13. Sections of seminiferous tubules of silver fox. (After Bishop.) (A) Regressed state of tubules following breeding season. (B) Tubule from fox during the breeding season, characterized by active spermatogenesis.

Fig. 14. Sections of the testis of the stickleback (Gasterosteus pungitius). (Modified from Moore, '39, after Van Oordt.) Cf. fig. 13, (A) Spermatogenic activity with many formed sperm in seminiferous tubules before the mating season, interstitial tissue in abeyance. (B) At mating period. Interstitial tissue well developed, spermatozoa stored in the tubules with spermatogenic activity absent.

Fig. 15. Seasonal reproductive cycle in the stickleback {Gasterosteus aculeatus). Cf. fig. 14. Breeding season is indicated by crosshatching below base line. Observe that spermatogenic activity follows rise of temperature, whereas interstitial-tissue and sexcharacter development occur during ascending period of light. (Redrawn from Turner: General Endocrinology, Philadelphia, Saunders, modified from Craig-Bennett, 1931.)

c. Testicular Control of Body Structure and Function by the Male Sex Hormone

1) Sources of the Male Sex Hormone. Testosterone is prepared from testicular extracts. It is the most potent of the androgens and is believed to be the hormone produced by the testis. The chemical formula of testosterone is:

The testis, however, is not the only site of androgen formation. As mentioned above, androgens are found in the urine of female animals, castrates, etc. It seems probable that the suprarenal (adrenal) cortex may secrete a certain androgenic substance, possibly adrenosterone, a weak androgen. Many androgens have been synthesized also in the laboratory (Schwenk, '44).

2) Biological Effects of the Male Sex Hormone. The presence of the male sex hormone in the male arouses the functional development of the accessory reproductive structures, the secondary sexual characters, and also stimulates the development of the seminiferous tubules. a) Effects upon the Accessory Reproductive Structures. Castration or removal of the testes from an animal possessing a continuous type of testicular activity produces shrinkage, and a general tendency toward atrophy, of the entire accessory reproductive structures. Injection of testosterone or other androgens under such conditions occasions a resurgence of functional development and enlargement of the accessory structures (fig. 16). Moreover, continued injections of the androgen will maintain the accessories in this functional state (Moore, '42; Dorfman in Pincus and Thimann, '50). Similarly, under normal conditions in those vertebrates which possess the seasonal type of testicular function, the accessory reproductive organs shrink in size with a loss of functional activity when the testis undergoes regression during the period immediately following the active season. An enlargement and acquisition of a normal functional condition of the accessories follows testicular development as the breeding season again approaches (Bishop, '42; Wislocki, '43; Matthews, '38; Turner, C. L., '19). (Compare figs. 12A-D.) b) Effects upon Secondary Sex Characteristics and Behavior of THE Individual. In addition to the primary effects upon the reproductive system itself, the androgens induce many other secondary structures and alterations of the physiology and behavior of the individual. The influence of the testicular hormone has been demonstrated in all of the vertebrate groups from fishes to mammals (Dorfman in Pincus and Thimann, '50). Examples of testosterone stimulation are: the singing and plumage of the male bird; hair development of certain mammals; the crowing and fighting, together with spur, comb, and wattle growth in the rooster. The disagreeable belligerency and positive energy drive of the bull, stallion, or human male may be attributed, largely, to the action of testicular hormone. However, lest we disparage this aggressive demeanor unduly, it should be recognized that upon such explosive force rests the preservation of species and races in some instances. As an example, witness that hairy dynamo of the barren northern tundras, the bull muskox, whose fiery pugnaciousness when the need arises undoubtedly has been a strong factor in the preservation of this species. An excellent example of the effect of testosterone is shown in the development of antlers and change in behavior of the Virginia deer, Odocoileus virginianus borealis (Wislocki, '43). In the northern climate, the testes and male accessory organs reach a profound condition of regression in April and May. Growth of the new antlers starts at this time, and during the late summer the antlers grow rapidly and begin to calcify. During the summer, also, the testes develop rapidly, and spermatogenesis results. Loss of the “velvet” covering of the antlers is experienced during September, and mating is the rule in October and November. The antlers are shed in midwinter. If the testes are removed after the naked antler condition is reached, the antlers are shed rapidly. Testosterone administered to does or to young males which have been castrated induces the development of antlers. The general scheme of antler development suggests, possibly, that the testicular hormone acts upon an anterior pituitary factor, and this activated factor in turn initiates antler growth. Hardening of the antlers and loss of velvet results from testosterone stimulation. Loss of the antler is synchronized with a decrease in the amount of testosterone in the blood stream, accompanied by the acquisition of a docile, non-belligerent, more timid behavior. c) Effects upon the Seminiferous Tubules. Testosterone has a stimulating effect upon the seminiferous tubule and sperm formation. This matter is discussed in Chap. 3. d. Seminiferous-tubule Activity and Formation of Sperm See Chap. 3. e. The Seminiferous Tubule as a Sperm-storing Structure See p. 31 .

3. Role of the Reproductive Duct in Sperm Formation

a. Vertebrates Without a Highly Tortuous Epididyrnal Portion of the Reproductive Duct

In a large number of vertebrates, morphologically developed sperm pass from the testis through the efferent ductules of the epididymis (vasa efferentia) to the epididyrnal duct where they remain for varying periods. However, in many vertebrates the anterior (proximal) portion of the sperm duct does not form a tortuous epididyrnal structure similar to that found in other vertebrates. This condition is present in the common frog, Rana; in the hellbender, Cryptobranchus; in the bowfin, Amia; etc. Because of this fact, the sperm pass directly into the vas deferens or sperm duct (Wolffian duct) without undergoing a sojourn through a convoluted epididyrnal portion of the duct. Correlated with the type of testis and sperm-duct relationship in the frog, is the fact that one may obtain viable, fertilizing sperm directly from the testis. For example, if one removes the testis from a living frog and macerates it in pond water or in an appropriate saline solution, active sperm are obtained which are capable of fertilizing eggs in a normal manner. That is, the frog testis matures sperm morphologically and physiologically. This type of testicular maturation is characteristic of many of the lower vertebrates possessing simple reproductive ducts.

Fig. 16. Effects of the male sex hormone upon the functional development of the accessory reproductive structures of the male rat. (After Turner: General Endocrinology , Philadelphia, Saunders, p. 324.) (A) Normal male rat condition produced by injection of crystalline male sex hormone for 20 days into castrate before autopsy. (B) Castrated male litter mate of (A) receiving no replacement therapy.

Fig. 17. Diagrammatic drawings of the two types of testicular-reproductive relationships occurring in the vertebrate group. (A) Simplified type of reproductive duct connected with the testis by means of efferent ductules. The duct-testis relationship of many telepst fishes is similar to this but does not possess the efferent ductules, the sinus-like reproductive duct being attached directly to the testis. Sperm cells (spermatozoa) are matured and stored within the testis. This type of relationship generally is found where fertilization is external or where sperm are discharged all at once during a short reproductive period. (B) More complicated variety of reproductive duct, connected with the testis by means of efferent ducts, but possessing an anterior twisted portion, the epididymal duct in which the sperm are stored and physiologically matured. This type of duct generally is found in those vertebrates which utilize internal fertilization and where sperm are discharged over a short or extended reproductive period.

b. The Epididymis as a Sperm-ripening Structure

On the other hand, in those forms which possess an anterior convoluted epididymal portion of the reproductive duct, the journey of the sperm through this portion of the duct appears to be necessary in order that fertilizable sperm may be produced. In mammals it has been shown that the epididymal journey somehow conditions the physiological ripening of the sperm. Sperm taken from the mammalian testis will not fertilize; those from the caudal portion of the epididymis will, provided they have been in the epididymis long enough. Under normal conditions sperm pass through the epididymis slowly, and retain their viability after many days' residence in this structure. Sperm prove to be fertile in the rabbit epididymis up to about the thirty-eighth day; if kept somewhat longer than this, they become senile and lose the ability to fertilize, although morphologically they may seem to be normal (Hammond and Asdell, '26). In the rat, they may live up to 20 to 30 days in the epididymis and still be capable of fertilization (Moore, '28). It has been estimated that the epididymal journey in the guinea pig consumes about two weeks, although they may live and retain their fertilizing power as long as 30 days in epididymides which have been isolated by constriction (Moore and McGee, '28; Young, '31; Young, '31b). It is said that in the bull, sperm within the epididymis may live and be motile for two months. As a result of these facts, it may be concluded that the epididymal journey normally is a slow process, and that it is beneficial for the development of sperm “ripeness” or ability to fertilize.

c. The Epididymis and Vas Deferens as Sperm-storage Organs

Along with the maturing faculty, the epididymal duct and vas deferens also act as sperm-storage organs. As observed on p. 23, in the bat, Myotis, sperm are formed in great numbers in the seminiferous tubules and pass to the epididymal duct where they are stored during the fall, winter, and early spring months; the epididymal journey thus is greatly prolonged in this species. In the ovoviviparous garter snake, Thamnophis radix, sperm are produced during the summer months; they pass into the epididymides during early autumn and are stored there during the fall and winter. In the mammal, sperm are stored in the epididymal duct. Aside from its main purpose of transporting sperm to the exterior (see sperm transport, p. 177), the caudal portion of the sperm duct or vas deferens also is capable of storing sperm for considerable periods of time. In the common perch, Perea ftavescens, sperm are developed in the testes in the autumn, pass gradually into the accessory reproductive ducts, and are stored there for five or six months until the breeding season the following spring (Turner, C. L., '19). Again, in mammals, the ampullary region of the vas deferens appears to be a site for sperm storage. For example, the ampulla of the bull sometimes is massaged through the rectal wall to obtain sperm for artificial insemination. In this form sperm may be stored in the ampulla and still be viable, for as long as three days. Similarly, in lower vertebrates large numbers of sperm may be found in the posterior extremities of the vas deferens during the breeding season. Thus, the reproductive duct (and its epididymal portion when present) is instrumental in many vertebrate species as a temporary storage place for the sperm.

d. Two Types of Vertebrate Testes Relative to Sperm Formation

The importance of the epididymal duct in many vertebrates and its relative absence in others, focuses attention upon the fact that in many vertebrate species sperm are produced, stored, and physiologically matured entirely within the confines of the testis (frog, bowfin, stickleback, etc.). The reproductive duct under these circumstances is used mainly for sperm transport. In many other vertebrate species sperm are morphologically formed in the testis and then are passed on into the accessory structures for storage and physiological maturation. Functionally, therefore, two types of testes and two types of accessory reproductive ducts are found among the vertebrate group of animals (fig. 17). It naturally follows that the testis which produces, stores, and physiologically matures sperm is best adapted for seasonal activity, particularly where one female is served during the reproductive activities. That is, it functions as an “all at one time” spawning mechanism. On the other hand, that testis which produces sperm morphologically and passes them on to a tortuous epididymal duct for storage and physiological maturing is best adapted for the continuous type of sperm production or for the service of several females during a single seasonal period. The sperm, under these conditions, pass slowly through the epididymal duct, and, therefore, may be discharged intermittently.

4. Function of the Seminal Vesicles (Vesicular Glands)

The seminal vesicles show much diversity in their distribution among various mammals. Forms like the cat, dog, opossum, rabbit, sloth, armadillo, whale, do not possess them, while in man, rat, elephant, mouse, they are welldeveloped structures. It was formerly thought that the seminal vesicles in mammals acted as a storehouse for the sperm, hence the name. In reality they are glandular structures which add their contents to the seminal fluid during the sexual act.

5. Function of the Prostate Gland

The prostate gland also is a variable structure and is found entirely in the marsupial and eutherian mammals. In marsupials it is confined to the prostatic portion of the urethral wall; in man it is a rounded, bulbous structure which surrounds the urethra close to the urinary bladder. In many other mammals it is a much smaller and less conspicuous structure. It discharges its contents into the seminal fluid during the orgasm. It is probable that the prostatic and vesicular fluids form the so-called “vaginal plug in the vagina of the rat, mouse, etc.

6. Bulbourethral (Cowper's) Glands

The bulbourethral glands are absent in the dog but present in most other mammals. In marsupials and monotremes these structures are exceptionally well formed. In the opossum there are three pairs of bulbourethral glands. The mucous contents of these and other small urethral glands are discharged at the beginning of the sexual climax and, as such, become part of the seminal fluid.

7. Functions of Seminal Fluid

a. Amount of Seminal Fluid Discharged and Its General Functions As stated previously, the semen or seminal fluid is composed of two parts, the sperm cells (spermia; spermatozoa) and the seminal plasma. The presence of the sperm cells represents the most constant feature, although they may vary considerably from species to species in size, shape, structure, and number present. The seminal plasma varies greatly as to composition and amount discharged. The quantity of seminal fluid discharged per ejaculate and the relative numbers of sperm present in man and a few other vertebrate species associated with him are as follows:*

Species Volume of Single Ejaculate, Most Common Value, in CC. Sperm Density in Semen, Average Value, per CC. Boar 250 CC. 100,000,000 per CC. Bull 4-5 CC. 1,000,000,000 per CC. Cock 0.8 CC. 3,500,000,000 per CC. Dog 6 CC. 200,000,000 per CC. Man 3.5 CC. 100,000,000 per CC. Rabbit 1 CC. 700,000,000 per CC. Ram 1 CC. 3,000,000,000 per CC. Stallion 70 CC. 120,000,000 per CC. Turkey 0.3 CC. 7,000,000,000 per CC.

• Modified from Mann ('50).

Two important branches of study involving the semen pertain to: (1) the chemical and physiological nature and numerical presence of the sperm, and (2) the physiology and biochemistry of the seminal plasma. (See Mann, '50, for discussion and bibliography.) As a result of the studies thus far, a considerable body of information has been accumulated. The main function of the semen, including the plasma and accessory sperm, appears to be to assist the sperm cell whose chance fortune it is to make contact with the egg. Once this association is accomplished, the egg seemingly takes over the problem of fertilization. The seminal plasma and the accessory numbers of sperm appear to act as an important protective bodyguard and also as an aid for this event. Modern research emphasizes, therefore, that the work of the male reproductive system is not complete until this contact is made.

b. Coagulation of the Semen In many mammalian species, the semen tends to coagulate after its discharge from the male system. In the mouse, rat, guinea pig, opossum, rhesus monkey, etc., the semen coagulates into a solid mass, the vaginal plug, once it reaches the vagina of the female. The probable function of the vaginal plug is to prevent the semen from seeping out of the vagina. The formation of this plug may be due to a protein present in the contents of the seminal vesicle which comes in contact with the enzyme, vesiculase. In the rat and guinea pig this catalyst probably is produced by the “coagulating gland,” a specialized structure associated with the seminal vesicles in these forms. Some of it also may come from the prostate. Coagulation of the seminal fluid also occurs in man, stallion, and boar but it is entirely absent in the dog, bull, and many other animals. Human semen coagulates immediately after discharge but liquefies a short time afterward. This liquefaction may be due to the presence of two enzymes, fibrinogenase and fibrinolysin, found in human semen and both derived from the prostate. These enzymes are found also in dog semen. In the latter their property of inhibiting blood coagulation may be of use where considerable amounts of blood may be present in the female genital tract at the onset of full estrous conditions. Another important contribution of the prostate gland is citric acid. Its role is not clear but it may enter into the above coagulation-liquefaction process (Mann, '50, p. 348).

c. Hyaluronidase Various enzymes have been demonstrated to be present in the semen of certain invertebrates and vertebrates. One such enzyme is hyaluronidase which appears to be produced in the testes of the rat, rabbit, boar, bull, and man. It is not found in the testes of vertebrates below the mammals. Its specific function is associated with the dispersal of the follicle cells surrounding the egg; in so doing it may aid the process of fertilization in mammals. d. Accessory Sperm One sperm normally effects a union with the egg in fertilization. Accessory sperm may enter large-yolked eggs, but only one is intimately involved in the union with the egg pronucleus. However, what is meant by accessory sperm here is the large number of sperm which normally clusters around the egg during the fertilization process in many animal species. A suggestion of a function for these accessory sperm follows from the fact that hyaluronidase may be extracted from the semen, presumably from the sperm themselves. Rowlands ('44) and also Leonard and Kurzrok ('46) have shown that a seminal fluid deficient in sperm numbers may fertilize if hyaluronidase extracted from sperm (?) is added to such a weakened sperm suspension. The implication is that the accessory sperm thus may act as “cupbearers” for the one successful sperm in that they carry hyaluronidase which aids in liquefying the follicle cells and other gelatinous coating material around the egg. e. Fructose An older concept in embryology maintained that sperm were unable to obtain or utilize nourishment after they departed from the testis. More recent investigation has shown, however, that sperm do utilize certain sugar materials, and that their survival depends upon the presence of a simple sugar in the medium in which they are kept. (See Mann, '50.) The sugar that is found normally in semen is fructose. It varies in quantity from species to species, being small in amount in the semen of the boar or stallion but considerably larger in quantity in the seminal fluid of the bull, man, and rabbit. The seat of origin of this sugar appears to be the seminal vesicle, at least in man, although the prostate may also be involved, particularly in the rabbit and also in the dog. The dog, however, has but a small amount of fructose in the seminal discharge. The real function of seminal fructose “might be as a readily utilizable store of energy for the survival of motile spermatozoa” (Mann, '50, p. 360). f. Enzyme-protecting Substances Runnstrom (personal communication) and his co-workers have demonstrated that the fertilizing life of sea-urchin sperm is increased by certain substances found in the jelly coat of the sea-urchin egg. Presumably these substances are protein in nature, and, according to Runnstrom, they may act to preserve the enzyme system of the sperm. Similarly, the seminal fluid may act to preserve the enzyme system of the sperm, while en route to the egg, especially within the female genital tract.

D. Internal and External Factors Influencing Activities of the Testis

Conditions which influence testicular activity are many. Many of the factors are unknown. Nevertheless, a few conditions which govern testis function have been determined, especially in certain mammalian species. The general results of experimental determination of some of the agents which affect testicular function are briefly outlined below.

1. Internal Factors

a. Temperature and Anatomical Position of the Testis

It is well known that in those mammals which have a permanent scrotal residence of the testes failure of the testis or testes to descend properly into the scrotum results in a corresponding failure of the seminiferous tubules to produce sperm. In these instances the testis may appear shriveled and shrunken (fig. 18). However, such cryptorchid (ectopic) conditions in most cases retain the ability to produce the sex hormone at least to some degree. A question therefore arises relative to the factors which inhibit seminiferous tubule activity within the cryptorchid testis.

The failure of cryptorchid testes to produce viable sperm has been of interest for a long time. Observations have demonstrated that the more hidden

Fig. 18. Experimental unilateral cryptorchidism in adult rat. The animal's left testis was confined within the abdominal cavity for six months, whereas the right testis was pernfitted to reside in the normal scrotal position. Observe the shrunken condition of the cryptorchid member. (After Turner: General Endocrinology, Philadelphia, Saunders.)

the testis (i.e., the nearer the peritoneal cavity) the less likely are mature sperm to be formed. A testis, in the lower inguinal canal or upper scrotal area is more normal in sperm production than one located in the upper inguinal canal or inside the inguinal ring. Studies made upon peritoneal and scrotal temperatures of rats, rabbits, guinea pigs, etc., demonstrate a temperature in the scrotum several degrees lower than that which obtains in the abdomen. These observations suggest that the higher temperature of the non-scrotal areas is a definite factor in bringing about seminiferous tubule injury and failure to produce sperm.

With this temperature factor in mind, Dr. Carl R. Moore (in Allen, Danforth, and Doisy, ’39) and others performed experiments designed to test its validity as a controlling influence. They found that confinement alone of an adult guinea pig testicle in the abdomen led to marked disorganization of all seminiferous tubules in seven days. After several months of such confinement the seminiferous tubules experience marked degenerative changes and only Sertoli cells remain (fig. 19A, B). The interstitial tissue, however, is not greatly impaired. If such a testis is kept not too long within the abnormal position and once again is returned to the scrotum, spermatogenesis is rejuvenated (fig. 20A, B). In a second experiment, the scrotum of a ram was encased loosely with insulating material; a rapid degeneration of the seminiferous tubules followed. Young (’27, ’29) in a third type of experiment found that water 6 to 7° warmer than the body temperature applied to the external aspect of the guinea-pig testis for a 15-minute period evoked degenerative

Fig. 19. Sections of experimental, cryptorchid, guinea-pig, seminiferous tubules and interstitial tissue. (Modified from C. R. Moore in Sex & Internal Secretions, Williams & Wilkins, Baltimore, 1939.) (A) Testis confined to abdomen for three months. (B)

Testis confined to abdomen for six months. Observe degenerate state of seminiferous tubule after six months’ confinement. Interstitial tissue not greatly affected by confinement.

changes with temporary sterility (fig. 21). Recovery, however, is the rule in the latter instance. Summarizing the effects of such experiments involving temperature, Moore (in Allen, Danforth, and Doisy, ’39, p. 371) concludes: “The injury developing from applied heat, although more rapidly effective, is entirely similar to that induced by the normal body temperature when the testicle is removed from the scrotum to the abdomen.”

The position of the scrotum and its anatomical structure is such as to enhance its purpose as a regulator of testicular temperature (figs. 2, 6). When the surrounding temperature is cold, the contraction of the dartos muscle tissue of the scrotal skin contracts the scrotum as a whole, while the contraction of the cremaster muscle loops pulls the testes and the scrotum closer to the body, thus conserving the contained heat. When the surrounding temperature is warm, these muscles relax, producing a more pendulous condition to permit heat loss from the scrotal wall.

In accordance with the foregoing description of the scrotum as a necessary thermoregulator for the testis, it has been further shown for those mammals which possess a scrotum that testis grafts fare much better when transplanted to the scrotal wall or into the anterior chamber of the eye (Turner, C. D., '48). The anterior chamber of the eyeball possesses a temperature much cooler than the internal parts of the body.

Fig. 20. Sections of testis during and after abdominal confinement. (Modified from C. R. Moore in Sex & Internal Secretions, Williams & Wilkins, Baltimore, 1939.) (A)

Section of left testis to show degenerate state of seminiferous tubules after 24 days of abdominal confinement. (B) Section of right testis 74 days after replacement in scrotum. Observe spermatogenic activity in tubules.

Fig. 21. Effect of higher temperature applied to external surface of guinea-pig testis. Water, 47®, was applied to surface of scrotum for period of 10 minutes. Testis was removed from animal 12 days after treatment. Seminiferous tubules are degenerate. (Modified from Moore, ’39; see also Young, ’27, J. Exp. Zool., 49.)

Two types of seminiferous tubules are thus found in mammals. In a few mammalian species (see p. 6) the temperature of the peritoneal cavity is favorable to the well-being of the seminiferous tubule; in most mammalian species, however, a lower temperature is required. On the other hand, the activities of the interstitial tissue of the testis appear to be much less sensitive to the surrounding temperature conditions, and the male sex hormone may be produced when the testes are removed from the scrotum and placed within the peritoneal cavity.

With regard to the functioning of the testis within the peritoneal cavity of birds it has been suggested that the air sacs may function to lower the temperature around the testis (Cowles and Nordstrom, ’46). In the sparrow, Riley (’37) found that mitotic activity in the testis is greatest during the early morning hours when the bird is resting and the body temperature is lower, by 3 or 4° C.

b. Body Nourishment in Relation to Testicular Function

The testis is a part of, and therefore dependent upon, the well-being of the body as a whole. However, as observed in the preceding pages the interstitial cells and their activities in the production of the male sex hormone are less sensitive to the internal environment of the body than are the seminiferous tubules.

The separation of these two phases of testicular function is well demonstrated during starvation and general inanition of the body as a whole. A falling off of sperm production is a definite result of starvation diets, although the germinative cells do not readily lose their ability to proliferate even after prolonged periods of starvation. But the interstitial cells and the cells of Sertoli are not as readily affected by inadequate diets or moderate starvation periods. Sex drive may be maintained in a starving animal, while his ability to produce mature, healthy sperm is lost. On the other hand, long periods of inanition also affect sex hormone production and the sexual interests of the animal.

Aside from the abundance of food in a well-rounded dietary regime, adequate supplies of various vitamins have been shown to be essential. Vitamin Bi is essential to the maintenance of the seminiferous tubules in pigeons. Pronounced degenerative changes in the seminiferous tubules of rats and other mammals occur in the absence of vitamins A and E (Mason, ’39). Prolonged absence of vitamin E produces an irreparable injury to the testis of rats; injury produced by vitamin A deficiency is reparable. The B-complex of vitamins seems to be especially important for the maintenance of the accessory reproductive structures, such as the prostate, seminal vesicles, etc. The absence of vitamin C has a general body effect, but does not influence the testis directly. Spme of these effects may be mediated through the pituitary gland. As vitamin D is intimately associated with the mineral metabolism of the body, it is not easy to demonstrate its direct importance.

c. The Hypophysis and Its Relation to Testicular Function

The word “hypophysis” literally means a process extending out below. The early anatomists regarded the hypophysis cerebri as a process of the brain more or less vestigial in character. It was long regarded as a structure through which waste materials from the brain filtered out through supposed openings into the nasal cavity. These wastes were in the form of mucus or phlegm, hence the name “pituitary,” derived from a Latin word meaning “mucus.” The word pituitary is often used synonymously with the word hypophysis.

The hypophysis is made up of the pars anterior or anterior lobe, pars intermedia or intermediate lobe, and a processus infundibuli or posterior lobe. The anterior lobe is a structure of great importance to the reproductive system; its removal (ablation) results in profound atrophic changes throughout the entire reproductive tract.

The importance of the pituitary gland in controlling reproductive phenomena was aroused by the work of Crowe, Cushing, and Homans (TO) and by Aschner (’12) who successfully removed the hypophysis of young dogs. One of the first fruits of this work was a demonstration of the lack of genital development when this organ was removed. Since that time many of the other cohabitants of man - rats, mice, cats, rabbits, etc. — have been hypophysectomized, and in all cases a rapid involution and atrophy of the genital structures results from pituitary removal. The testis undergoes profound shrinkage and regression following hypophysectomy, the degree of change* varying with the species. In the rooster and monkey, for example, regressive changes are more marked than in the rat. (Consult Smith, ’39, for data and references.)

A striking demonstration of the influence of the hypophysis upon the genital tract is the result of its removal from a seasonal-breeding species, such as the ferret. Ablation of the pituitary in this species during the nonbreeding season causes slight if any change in the testis and accessory reproductive organs. However, when it is removed during the breeding season, a marked regression to a condition similar to that present during the nonbreeding season occurs (Hill and Parkes, ’33).

The experimental result of hypophysectomy on many animal species thus points directly to this structure as the site of hormonal secretion, particularly to the anterior lobe (Smith, ’39). The initial work on the relation of pituitary hormones and the gonad was done upon the female animal. The results of these studies aroused the question whether one or two hormones were responsible. The latter alternative was suggested by the work of Aschheim and Zondek (’27) and Zondek (’30) who concluded that two separate substances appeared to be concerned with the control of ovarian changes.

Nevertheless, for a time the concept of only one gonad -con trolling (gonadotrophic) hormone was produced by the pituitary, continued to gain attention, and some workers suggested that the two ovarian elfects of follicular growth and luteinization of the follicle were due to the length of time of administration of one hormone and not to two separate substances. However, this position soon was made untenable by research upon the gonadotrophic substances derived from the pituitary gland. Studies along this line by Fevold, Hisaw, and Leonard (’31) and Fevold and Hisaw (’34) reported the fractionation, from pituitary gland sources, of two gonadotrophic substances, a follicle-stimulating factor or FSH and a luteinization factor or LH. This work has been extensively confirmed. It should be observed in passing that the male pituitary gland contains large amounts of FSH, although, as mentioned below, the function of the testis and the male reproductive system relies to a great extent upon the luteinizing factor. Some investigators refer to the LH factor as the interstitial-cell-stimulating hormone, ICSH. (See Evans, ’47; and also Evans and Simpson in Pincus and Thimann, ’50.)

The action of these two hormones upon testicular tissue, according to present information, is somewhat as follows: If pure follicle-stimulating hormone, FSH, which produces only FSH effects in the female, is injected in low doses into hypophysectomized male rats, the seminiferous tubules are stimulated and spermatogenesis occurs. Under these conditions, the interstitial tissue remains unstimulated and the accessories continue in an atrophic state. It has further been demonstrated that slight amounts of the luteinizing gonadotrophic hormone, LH (ICSH), added to the above injections of FSH, effects a much better stimulation of the spermatogonial tissue, and the interstitial tissue also develops well.

On the other hand, when pure LH (ICSH) is given alone in small doses, spermatogenesis is stimulated with slight or no effect upon the male accessory structures. However, when larger doses of the LH (ICSH) factor alone are injected, the interstitial tissue is greatly stimulated, and the testicular weight increases much more than when FSH alone is given. Furthermore, the accessory reproductive structures are stimulated and become well developed, suggesting the elaboration of the male sex hormone. In agreement with these results, the administration alone of testosterone, the male sex hormone, increases the weight and development of the accessory structures in hypophysectomized animals and it also maintains spermatogenesis. It appears, therefore, that the effects of the LH substance upon the seminiferous tubules and the accessory organs occur by means of its ability to arouse the formation of the male sex hormone.

A summary of the actions of the pituitary gonadotrophic hormones upon testicular tissue may be stated as follows:

1. Pure FSH in small doses stimulates the seminiferous tubules and spermatogenesis with little or no effect upon the interstitial tissue or the accessory reproductive structures, such as the seminal vesicles or prostate gland;
2. Small doses of pure LH also stimulate spermatogenesis with little or no stimulation of the accessory structures;
3. Pure LH (ICSH) in larger doses stimulates the development of the interstitial tissue with the subsequent secretion of the male sex hormone and hypertrophy of the accessory reproductive organs;
4. The male sex hormone in some way aids or stimulates the process of spermatogenesis, suggesting that the action of LH occurs through the medium of the sex hormone (fig. 22).

(Consult Evans and Simpson in Pincus and Thimann, ’50, for data and references; also Turner, C. D., ’48.)

The foregoing results of the action of the FSH and LH upon testicular function might suggest that the LH substance alone is essential in the male animal. However, it should be observed that without the presence of FSH, LH is not able to maintain the tubules in a strictly normal manner, the tubules showing a diminution of size. Also, in extreme atrophic conditions of the tubules, pure FSH stimulates spermatogenesis better than similar quantities of LH. It is probable that FSH and LH (ICSH) work together to effect complete normality in the male. This combined effect is known as a synergistic effect. It also is of interest that the injection of small doses of testosterone propionate into the normal male, with the pituitary gland intact, results in inhibition of the seminiferous tubules, probably due to the suppression of pituitary secretion by the increased atnount of the male sex hormone in the blood. However, high doses, while they likewise inhibit the pituitary, result in a level of androgen which stimulates the seminiferous tubules directly (Ludwig, ’50).

Aside from the above actions upon testicular tissue by the luteinizing hormone (LH;ICSH) certain other functions of this substance should be mentioned (see fig. 22). One of these is the apparent dependence of the Sertoli cells upon the presence of the interstitial cells (Williams, ’50). Interstitial tissue behavior and development in turn relies mainly upon LH (ICSH) (Fevold, ’39; Evans and Simpson in Pincus and Thimann, ’50). As the sperm are intimately associated with the Sertoli elements during the latter phases of spermatogenesis in which they transform from the spermatid into the form of the adult sperm, a very close association and reliance upon the presence of the luteinizing hormone thus appears to be established in sperm development.

A further study of the LH factor is associated with the maintenance of the seminiferous tubules themselves. In aged males, the interstitial tissue and the seminiferous tubules normally involute and regress with accumulation of large amounts of connective tissue material. In testicular grafts made into the rabbit’s ear, Williams (’50) found, when interstitial tissue was present in the grafts, the seminiferous tubules were more nearly normal; when absent, the tubules underwent fibrosis.

Another function of the LH substance apparently is concerned with release of the sperm from the Sertoli cells. De Robertis, et al. (’46), showed that anterior pituitary hormones possibly cause release of sperm from the Sertoli cells in the toad by the production of vacuoles and apical destruction of the cytoplasm of the Sertoli elements. In testicular grafts Williams (’50) accumulated evidence which suggests that vacuoles and secretion droplets in the Sertoli cells occurred as a result of LH administration. The combined results of these investigators suggest that sperm release from the Sertoli cell is dependent, in some way, upon LH (ICSH) activity.

A final function is concerned with the physiological maturing of sperm in the reproductive duct, at least in many vertebrate species. The well-being of the epididymis and vas deferens is dependent upon the presence of the male sex hormone (Creep, Fevold, and Hisaw, ’36). As the male sex hormone results from stimulation of the interstitial cells by the interstitial-cellstimulating substance, LH (ICSH), the connection between this substance and the physiological maturation of the sperm cell is obvious.

2. External Environmental Factors and Testis Function

As we have seen above, the anterior lobe of the hypophysis acts as the main internal environmental factor controlling the testes and, through them, the reproductive ducts. It has been observed also that food, vitamins, and anatomical position of the testis are important influences in regulating testicular function. Furthermore, general physiological conditions such as health or disease have an important bearing upon the gonads (Mills, ’19). All of the above conditions are contained within the body of the organism, and as such represent organismal conditions.

[[File:Nelsen1953 fig030.jpg|600px

Fig. 22. Chart showing the effects of the hypophyseal anterior lobe upon the developing gametes. It also suggests the various factors influencing pituitary secretion of the gonadotrophic hormones, FSH and LH. Observe that the primitive gamete in the cortex of the ovary is subjected to the cortical environment and develops into an oocyte, whereas in the medullary or testicular environment it develops into a spermatocyte. Experiments upon sex reversal have demonstrated that the medullary and cortical portions of the gonad determine the fate of the germ cell. In the male area or medulla, the germ cell differentiates in the male direction, while in the cortex, the differentiation is in the direction of the female gamete or oocyte, regardless of the innate sex-chromosome constitution of the primitive germ cell. The fate of the germ cell thus is influenced by four main sets of factors: (1) Internal and external environmental factors, controlling the secretions of the pituitary body, (2) Fnvironment of the testicular tissue (medulla) and possible humoral substances produced in this tissue, (3) Environment of the ovarian tissue (cortex) and possible humoral substances elaborated there, and (4) Secretions of the anterior lobe of the pituitary body.

The following question naturally arises: Do factors or conditions external to the body impinge themselves in such a way as to control pituitary and gonadal function?

a. Light as a Factor

Aside from the supply of nutritive substances or the collision of the many nervous stimuli with the individual which may arouse or depress the sexual activities, two of the most important obvious external factors are temperature and light. Research on the reproductive behavior of many animal species, during the past twenty years, has shown that both of these factors have great significance on the reproductive activities of many vertebrate species. Bissonnette (’30, ’32, ’35, a and b) has accumulated evidence which demonstrates that light is a potent factor in controlling the reproductive behavior of the European starling (Sturnus vulgaris) and also of the ferret (Putorius vulgaris). In the starling, for example, the evidence shows that green wave lengths of the spectrum inhibit testicular activity, while red rays and white light arouse the reproductive function (fig. 23). The addition of electric lighting to each day’s duration produced a total testis size in midwinter which surpassed the normal condition in the spring. In the ferret artificially increased day length beginning at the first part of October brings the testis to maximum size and activity coupled with a normal mating impulse as early as November and December (fig. 24). Under normal conditions the male ferret is able to breed only during February and early March,

These findings relative to the influence of light on the reproductive periodicity of animals confirm a fact which has been known for a long time, namely, that seasonal breeders brought from the northern hemisphere to the southern hemisphere reverse their breeding season. For example, ferrets which normally breed from spring to summer in the northern hemisphere shift their breeding habits to the September-February period when moved to the southern hemisphere. Inasmuch as the hypophysis is instrumental in bringing about secretion of the gonadotrophic hormones responsible for the testicular activity, it is highly probable that light coming through the eyes (see Hill and Parkes, ’33) influences the nervous system in some way arousing the hypophysis and stimulating it to secrete these substances in greater quantity. However, one must keep in mind the caution given by Bissonnette, that light is not the only factor conditioning the sexual cycles of ferrets and starlings.

While numerous animals, such as the migratory birds, ferret, mare, many fish, frogs, etc., normally are brought into a breeding condition during the period of light ascendency, a large number of animals experience a sexual resurgence only during the time of year when the light of day is regressing in span. This condition is found in some sheep, goats, buffalo in nature.

Fig. 23. Sections of testis of the starling (Sturnus vulgaris), showing the effect of electric lighting added to the bird’s normal daily duration of light during the autumn. (After Bissonnette, Physiol. Zool., 4.) (A) Inside young control bird — no light added

— kept inside as control for (B) from November 9 to December 13. (B) Inside young

experimental bird, receiving additional light from “25 watt” bulb from November 9 to December 13. Total treatment, 34 davs.

Fig. 24. Sections of testis and epididymis, showing modification of sexual cycle in the ferret, Putorius vulgaris, by exposure to increasing periods of light. (After Bissonnette, ’35b.) (A) Seminiferous tubules from normal male over 1 year old, made on October

3, no lighting. (B) Epididymis of normal male on October 3, no lighting. (C) Seminiferous tubules of experimental male on November 7, 36 days of added lighting. (D) Epididymis of experimental males on Nov Tiber 7, 36 days of added lighting.

deer, some fish, etc. Bissonnette (’41) working with goats found that: “Increasing daily light periods from January 25 to April 5 — followed by diminishing periods until July 5, while temperatures remained normal for the seasons, with four Toggenburg female goats and one male Toggenburg and one Nubian female — led to cessation of breeding cycles in February instead of March, followed by initiation of breeding cycles in May and June instead of September.” In the ewe, Yeates (’47) also found that a change from increasing daylight to decreasing length of day induced reproductive activity. In a similar manner. Hoover and Hubbard (’37) were able to modify the sexual cycle in a variety of brook trout which normally breeds in December to a breeding season in August.

b. Temperature Influences

In the case of the animals mentioned above, temperature does not appear to be a major factor in inducing reproductive activity. However, in many animals temperature is vitally influential in this respect. For example, in the thirteen-lined spermophile (ground squirrel) Wells (’35) observed that breeding males kept at 40° F. continued in a breeding condition throughout the year. Under normal conditions this rodent hibernates during the winter months and comes forth in the spring ready to breed; sperm proliferation and general reproductive development take place during the period of hibernation. As the temperature rises during the spring and summer, testicular atrophy ensues, followed by a period of spermatogenesis and reproductive activity when the lowered temperatures of autumn and winter come again. Light, seemingly, is not a factor in this sexual cycle. Another instance of temperature control occurs in the sexual phase of the common red newt, Triturus viriciescens. Here it is the rising temperature of the summer which acts as the inducing agent, and sperm thus produced are discharged into the accessory ducts during the fall and winter to be used when copulation occurs in early spring. However, if this species is kept at a relatively low temperature of 8 to 12° C. during the summer months, spermatogenesis is inhibited and the testis regresses. In the stickleback, Gasterosteus aculeatus, as reported by Craig-Bennett (’31), spermatogenesis occurs during July to early September and appears to be conditioned by a rising temperature, whereas the interstitial tissue and the appearance of secondary sexual features reach their greatest development under increased light conditions and slowly rising temperatures (fig. 15). Bissonnette, in his work on ferrets, also observed a difference in the behavior of these two testicular components; the interstitial tissue responds to large increases of daily light periods, whereas the seminiferous tubules are stimulated by small, gradually increasing periods of light.

The above examples emphasize the importance of a single environmental factor on the pituitary-gonadal relationship. However, in the hedgehog, Allanson and Deansley (’34) emphasize temperature, lighting, and hormone injections as factors modifying the sexual cycles, while Baker and Ransom (’32, ’33, a and b) show that light, food, temperature, and locality affect the sexual cycles and breeding habits of the field mouse. In some vertebrates, therefore, a single factor may be the dominant one, whereas in others, numerous factors control the action of the pituitary and reproductive system.

E. Internal Factors Which May Control Seasonal and Continuous Types of Testicular Function

In endeavoring to explain the differences in response to external environmental factors on the part of seasonal and continuous breeders, one must keep in mind the following possibilities:

(1) The anterior lobe of the hypophysis in some forms (e.g., ferret) cannot be maintained in a secretory condition after it has reached its climax; that is, it apparently becomes insensitive to the light factor. As a result, regression of the pituitary and testis occurs (Bissonnette, ’35b).

(2) In the starling, the anterior hypophysis may be maintained by the lighting, but the testis itself does not respond to the presence of the hypophyseal hormones in the blood (Bissonnette, ’35b). The possibility in this instance may be that testicular function wanes because the body rapidly eliminates the hormone in some way (see Bachman, Collip, and Selye, ’34).

(3) Consideration also must be given to the suggestion that the activities of the sex gland by the secretion of the sex hormone may suppress anterior lobe activity (Moore and Price, ’32).

We may consider two further possibilities relative to continuous testicular function :

(4) If the “brake actions” mentioned above are not present or present only in a slight degree, a degree not sufficient to interrupt the activities of the anterior lobe or of the sex gland, a more or less continuous function of the testis may be maintained.

(5) When several or many environmental factors are concerned in producing testicular activity, a slight altering of one factor, such as light, may prove insufficient to interrupt the pituitary-germ-gland relationship, and a continuous breeding state is effected in spite of seasonal changes.

Underlying the above possibilities which may control testicular function is the inherent tendency or hereditary constitution of the animal. In the final analysis, it is this constitution which responds to environmental stimuli, and moreover, controls the entire metabolism of the body. In other words, the above-mentioned possibilities tend to oversimplify the problem. The organism as a whole must be considered; reproduction is not merely an environmentalpituitary-sex gland relationship.

F. Characteristics of the Male Reproductive Cycle and Its Relation to Reproductive Conditions in the Female

As indicated above, reproduction in the male vertebrate is either a continuous process throughout the reproductive life of the individual or it is a discontinuous, periodic affair. In the continuous form of reproduction the activities of the seminiferous tubules and the interstitial or hormone-producing tissues of the testis function side by side in a continuous fashion. In the discontinuous, periodic type of testicular function, the activities of the seminiferous tubules and of the interstitial tissue do not always coincide. The activities of the seminiferous tubules, resulting in the production of sperm for a particular reproductive cycle, tend to precede, in some species by many months, the activities of the sex-hormone-producing tissue. Evidently, the output of the FSH and LH substances from the pituitary gland are spread out over different periods of the year to harmonize with this activity of the testicular components.

It will be seen in the next chapter that a continuous breeding faculty is not present in the female comparable to that of the male. All females are discontinuous breeders. In some species, the cycles follow each other with little rest between each cycle unless the female becomes pregnant or “broody.” Some have a series of cycles over one part of the year but experience sexual quiescence over the remaining portion of the year. However, in most female vertebrates there is but one reproductive cycle per year.

In harmony with the above conditions, the continuous variety of testicular function is always associated with the condition in the female where more than one reproductive cycle occurs per year. Continuous reproductive conditions in the male, therefore, are adapted to serve one female two or more times per year or several different females at intervals through the year. Furthermore, the complicated, highly glandular, greatly extended type of male-reproductive-duct system is adapted to conditions of (1) continuous breeding, or (2) service to more than one female during one breeding season of the year, whereas the simple type of reproductive duct is adapted to the type of service where all or most of the genital products are discharged during one brief period. In other words, the entire male reproductive system and reproductive habits are adapted to the behavior of female reproductive activities.

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