Paper - Development of the Mouse Gonads 4

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Rowlands IW. and Brambell FWR. The development and morphology of the gonads of the mouse. Part IV. The post-natal growth of the testis. (1932) : 200-213.

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This historic 1928 paper by Rowlands and Brambell is the fourth in a series investigating the development of the mouse gonad.



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


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The Development and Morphology of the Gonads of the Mouse. IV. The Post-Natal Growth of the Testis

Francis William Rogers Brambell (1901 – 1970)

By I. W. Rowlands and F. W. Rogers Brambell.


From the Department of Zoolology University College of North Wales, Bangor.

Communicated by Sir Henry Dale, See. R.S.— Received August 16, 1932. Revised November 9, 1932.

Introduction

The early development of the gonads of the mouse, including the difierentiar tion of the ovary and testis, was described by Brambell (1927) in the first part of this series, together with the subsequent development of the ovary. It was intended to describe in a subsequent paper the development of the testis from the time of its difiercntiation until maturity, but examination of an extensive series of embryonic testes did not yield results of sufficient importance to require publication, since the paper by Agdhur (1927), dealing with this subject, had appeared in the meantime. The present paper deals with the development of the testis from birth until long after sexual maturity is attained, and is, therefore, the logical completion of the series begun in 1927.


This paper deals chiefly with the sizes of the testes and their measurable components in relation to the age and the cleaned-body weight. The results, so obtained, are correlated with the more clearly defined histological phases, but no attempt is made to describe systematically the post—natal histology or cytology of the testis.


The work has been executed with a View to providing data of the normal growth of the testis in the mouse, such as Donaldson (1924) has provided for the rat, which should serve as controls for experimental work. In particular an attempt has been made to treat separately the growth of two component tissues of the te.stis—the spermatic tubules and the intertubular tissue. We define the “intertubular” tissue as all tissues within the tunica albuginea other than the spermatic tubules. It therefore includes connective tissue, bloodvessels, lymph-spaces, etc-., as well as the so-called “interstitial” cells. It was found impossible to measure accurately the amount of interstitial cells present.

Material

Albino mice were employed because they provide suitable material for subsequent experimental work and because they have no restricted breeding season or correlated seasonal enlargement in the reproductive organs.


All the animals employed were derived from the colony in this department, which is an ofi-shoot of the in-bred colony employed by Parkes (1926). We would like to take this opportunity of expressing our thanks to Dr. A. S. Parkes for providing the animals from which our colony has been raised. Care was taken to insure that the diet was uniform and adequate.


Litters of mice are usually born during the night and are consequently some hours old when first observed in the morning. They were considered to be half a day old on the morning after birth in all cases.


The expenses of this research were defrayed in part by a grant from the Government Grant Committee of the Royal Society to one of us (F.W.R.B.), for which we wish to express our thanks.

Technique

(a) Method of Weighing

The cleaned-body weight was employed in preference to the entire-body weight as being more constant and not affected by the state of distention of the gut and bladder. The stomach and intestine were removed for this purpose, after ligaturing the coaliac artery and the portal vein, and the bladder was evacuated.


The testes were weighed separately in weighing bottles, after the removal of the epididymis and of all fat from each. The weights were checked by taking the combined weight of the two testes after transferring one testis to the bottle containing the other. This involved a slight loss in weight through loss of moisture condensed on the first bottle.


(b) Histological Treatment

The testes were immersed in fixative as soon as possible after weighing. In no case did more than 15 minutes elapse between killing and immersion in the fixative. Bouin’s fluid was always employed, except that for the larger testes the modified alcoholic fluid, in which a saturated solution of picric acid in 70 per cent. alcohol is substituted for the saturated aqueous solution, was used. This modification was necessary to ensure rapid penetration, since it was not possible to cut the tunica albuginea. and thus hasten penetration, as this would have afiected the size relations of the tissues. Care was taken to standardize so far as possible the fixation and subsequent treatment of the testes, since small variations in technique introduce an uncontrollable error in subsequent measurements through producing different amounts of shrinkage in the tissues. Complete serial sections, cut transversely at 10 in. thick, were made of one testis of each animal, and were stained with Ehrlich’s haamatoxylin and eosin.


(c) Measurement of Tissues

Drawings were made, at a magnification of 100 diameters, by means of a Leitz micro-projection apparatus, of the largest transverse section of each testis. The diameter of each tubule and the total number cut across was determined from these drawings. Since many tubules are cut tangentially in a transverse section and appear elliptical the diameter of each was taken as the greatest width at right angles to the long axis of the ellipse. The mean diameter of all the tubules in the greatest transverse section, measured in this way, was determined for each testis.


The total area of the spermatic tubules and of the intertubular tissue was also estimated from these drawings. This was done by cutting out and weighing the drawing, then cutting out all the tubules, weighing them and the residue of the paper. The weights were subsequently converted to estimates of area by employing as standard the weight of a known area of the same paper, which was assumed to be uniform.

(d) Treatment of Results

The results obtained are, with the exception of the relation of the weight of the right testis to that of the left, presented in the form of scatter diagrams. These bring out the relevant points concerning the growth changes, and possess at the same time the advantage of rendering all the data available for statistical analyses. It was found impracticable to fit curves represented by polynomial terms since the data were unequally spaced.


The data of the relative weights of the right and left testes were treated as a straight line regression.

We are indebted to Dr. A. S. Parkes, Dr. J. Wishart and Dr. F. G. Soper for advice and criticism.


Observations

Post-natal Growth in Body—weight

During the course of the researches on the growth of the testis data of the cleaned-body weight and age of one hundred male mice, ranging from newly born to animals 300 days old, were accumulated. These data, fig. 1, are sufficient to determine the general form of the growth in cleaned-body weight on age, which has an important bearing on the interpretation of the changes described in the testis. It is not the purpose of this paper to deal with growth in body-weight as such or to offer any theoretical interpretation of the form of the growth-curve, for which purpose more extensive data would be desirable.


fig. 1.

Post-natal Growth of the Testes

(a) Relation of Weight of Testes to Cleaned-body Weight.I.— The data available consisted of accurate. weights of 115 animals ranging from 1 to 33 gm. cleanedbody weight. They are given in fig. 2 in the form of a scatter diagram.

(b) Relation of Weight of Testes to Age.-——The data, consisting of the weights of the testes of 101 animals of known age ranging from birth to 300 days, are given in fig. 3.

(c) Relation of the Weight of the Testes expressed as a Pevrcentage of the CIeam'.dbody Weight to Age.——The data, derived from the same 101 animals as in section (b) are given in fig. 4. It can be seen that the percentage weight of the testes rises rapidly from about 10 to 40 days old, when the maximum is attained. Subsequently the percentage weight of the testes remains constant throughout life at a value of approximately 0 -85 per cent. body weight.


I. W. Rowlands and F. ‘W. R. Bramhell.


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°II’e*1'gvhla/‘testes in 9/52.

Age in day: Fm. 3.


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Age m days‘ Fm. 4.



(d) Size af Right and Left Testes.—-Comparison of the weights of the right and left testes of 92 pairs showed :—

Right > left . . . . . . . . . . . . 76 Right = left . . . . . . . . . . . . - 3 Right <1eft . . . . . 13

The data were fitted with a straight regression line for the weight of the right testis on the weight of the left testis. The regression is expressed by the formula Y = 1 -0334 re, where Y = weight of the right testis and 1: the weight of the left testis in grams. Testing the significance of the differeiice between this regression coefiicient and the hypothetical value, i.e., Y = X, where the two testes are of equal weight t = 7 -57 and n = 90. Entering fisher’s (1930) table of t with these values P is found to be less than 0-01 and the difference between the two regressions must be considered decidedly significant. The regression line is represented by a continuous line in fig. 5, and the hypothetical regression line, if the weights of the two testes tended to equality, is represented by the dotted line.

fiG. 5.

Post-natal Growth of the Component Parts of the Testis

(a) Increase in Dmmeter of the Spermalic TubuIes.—The data. consist of the mean diameters of the tubules in the testes of 80 animals of known ages from birth to 300 days. The mean diameter of all the tubules in a. single transverse section across the middle of one testis was taken in each case as the diameter of the tubules in that animal. The data are represented in fig. 6.


Moan diam nf.r

O )0 I00 90 200 230 )00 Age 1 n day:

fiG. 6.


It can be seen that there is little or no appreciable increase in the diameter of the tubules after the 40th day. (6) Number and Area of Spermatic Tubules in Transverse Sections.—The number of spermatic tubules cut across in a transverse section of the testis appears to remain approximately constant from shortly after birth until maturity. This is shown by the correlation table.

Correlation Table

Number of Age in days.

spermatic tubules in transverse section. 10-1 9 - 9 .

4049-9. 50-594). 60-69-0. 70<.


20--29 - 9. F 30-39 -9.


250-274-9 225-249-9 200-2240 175-1994) 150-174-fl 125-149-9 100-124-9

.—! ls'at\'.>6's| . l 3 3 l

|»—|¢.:-lea] llllwll

T 2 1

lllwlll

The constant number of spermatic tubules in a transverse section, which implies also that they do not become more convoluted, since this would result in a consequent increase in the number of times they would be cut across, is also brought out by the data of the total areas of the spermatic tubules in transverse section. These data are available for 62 animals, ranging in age from 10 to 300 days, in which the mean diameter of the spermatic tubules was lmown. The total area of the spermatic tubules is plotted against the square of the mean diameter for 62 animals fig. 7. It is obvious that the data tend to fall on a straight line, thus showing that the total area of the spermatic tubules in a transverse section of the testis is a constant function of the square of the mean diameter. Expressed in other words the number of tubules cut across in a transverse section of the testis is constant from 10 to 300 days old.

(c) Area of the Intertubular Tissue.—The data consist of measurements of the total area of intertubular tissue in the largest transverse section of one testis of each of 56 animals of known ages from 10 to 200 days. These data

are given in fig. 8, and indicate a gradual falling ofi in the rate of increase of the area of the intertubular tissue with increasing age.

(41) Relative Area of Tubular to I ntertubular Tissue.—The data, fig. 9, consist of the area of the intertubular tissue divided by the area of the spermatic tubules in 62 animals between 10 and 300 days old. It can be seen that the relative area reaches a minimum at about 30 to 40 days old, and subsequently rises to a higher level. Small inequalities in the histological technique probably result in difierential shrinkage of the tubular and intertubular tissue and account for the wide spread of the data.


7: in T51 oflesgls in mm m.

Tolalaneauafspor-maiic lugules

, -on -02 «O3 01 /Ales» diam)’ afspermallc tubules in so In 01

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Ar-ea af'inte/-tubular tissué m Z'.S‘.of(¢,;t£.r in .90 mm, u

Age in dayr



0 I00 200 300

Age 1'}: day: fiG. 9.

Re! .z_l 1' re arm afinfgrlubularla lubgzlarlisxuain Hqflafis

Spermatogenesis in Relation to Age

The testes of 60 mice, ranging from birth to maturity, were examined histologically with a view to determining the time relations of the more salient points in the process of spermatogenesis. For this purpose clearly defined phases, such as pachynema, the maturation spindles, spermatids and ripe spermatozoa, were chosen and the ages at which cells in these stages first appeared and reached a maximum number were determined. The material employed consisted of the testes of one or more animals at daily age intervals from birth to 45 days old, with others at 50, 60 and 76 days old, and two animals upwards of one year old.


The spermatic tubules in the new-born mouse are solid and the contained germ-cells are spermatogonia and primary spermatocytes. Some of the Bpermatogonia are in mitosis and the primary spermatocytes are in the deute-broch stage. Spermatocytes with pachytene nuclei appear early and reach a maximum on the 13th-14th day when they are very numerous and form a layer three or four cells thick in the tubule. Subsequently, though always present, pachytene nuclei are less numerous. A lumen first appears in some of the tubules on the 13th day, and in a day or two is present in all. After this time spermatogenesis appears to proceed more actively in some tubules than in others. Soon heterotypic spindles appear and the first maturation division takes place. On the 18th day some of the tubules exhibit heterotypio spindles while in others the first maturation division is completed and secondary spermatocytes are present. The secondary spermatocytes do not enter upon a resting stage, so that the second maturation division follows soon after the first, and spermatids are found in the tubules by the 20th day. At this time the seminal epithelium consists of a single row of spcrmatogonia next the wall of the tubule, then a row of primary spermatocytes followed by a layer of secondary spermatocytes, two or more cells thick, and finally a row of spermatids next to the lumen.


The first indications of sperrnateleosis, or the metamorphosis of the spermatids into spermatozoa, are discernible by the 21st day, and by the 30th day this process is taking place in many cells. At the age of 33 to 35 days immature spermatozoa with tails are present attached to the Sertoli cells by their acrosomes, but still retaining the cytoplasm of the spermatid which is subsequently sloughed ofi. Immature spermatozoa are very numerous and some are in process of sloughing off the residual cytoplasm by the 40th day. Mature spermatozoa, free in the lumen of the tubules, are found first at the age of 42 days. Testes at 45 and 50 days old showed large numbers of mature sperms together with a further lot of spermatids in spermateleosis. At 60 days sperms were present in the lumina of the efferent tubules but may have been present here a few days earlier. Spermatogenesis was still proceeding actively in the testes over a year old. No marked wave of degeneration in the germ-cells, such as has been recorded in a number of other mammals shortly before puberty, was observed at any stage between birth and maturity in the mice examined.

Discussion

The increase in weight of the two testes is given both in relation to cleanedbody weight and to age. It can be seen that the most rapid increase in the weight of the testes occurs at a body weight of 10 to 12 gm., fig. 2, and at an age of 30 to 40 days, fig. 3. Further the rate of increase in the weight of the testes drops ofi rapidly after about 60 days. The diagram of the percentage body weight of the testes on age, fig. 4, brings out an interesting relation. The data from 10 to 40 days approximate to a straight line relationship indicating a constant rate of increase in the percentage body weight of the testes over this period. Subsequently the percentage body weight of the testes appears to remain constant at approximately 0-85 per cent. body weight.


The fact that the right testis tends to be significantly heavier than the left is clearly shown in fig. 5.


The diagram of the mean diameter of the spermatic tubules on age shows a maximum rate of increase at about a fortnight old. It can be seen from fig. 6 that the curve begins to flatten out at 40 days, and that, subsequently, there is little or no perceptible increase in the diameter of the tubules. It is remarkable that the mean number of spermatic tubules cut across in a transverse section through the middle of the testis appears to remain approximately constant from 10 days old, although the actual number is variable within fairly wide limits. This is also shown by the fact that data of the total area of the spermatic tubules in single transverse sections of the testis plotted against the square of the mean diameter fall on a straight line, fig. 7. The total area of the spermatic tubules in a transverse section is, in fact, a constant function of their mean diameter.


The increase in the area of intertubular tissue with age is shown in fig. 8. We have defined the intertubular tissue as all the tissue within the tunica albuginea other than the spermatic tubules. It is thus an artificial conception. including blood vessels, lymph spaces, connective tissue, etc., together with the so-called “ interstitia ” cells. Technical difiiculties rendered it impossible to arrive at an estimate of the area of the “interstitial” tissue alone with suflicient accuracy. The relative importance of the spermatic tubules and theintertubular tissue as components of the testis is brought out by fig. 9 in which the values of the area of intertubular tissue divided by the area of the spermatie tubules are plotted against age. It can be seen that a minimal value is reached at 30 to 40 days and rises subsequently. It is perhaps significant that Kasai (1908) found two maxima in the growth of the “interstitial "' tissue in the human testis respectively at the 7th month of foetal life and at puberty.


Considering the more characteristic and clearly defined phases of spermatogenesis it can be seen that primary spermatocytes are already present in the testis of the new-bom mouse. The number of nuclei in pachynema reaches :1 maximum on the 13th or 14th day. Simultaneously with the appearance of the maximum number of pachytene nuclei, a lumen first appears in the spermatic tubules, which were previously solid. Spermatids are found first on the 20th day and mature spermatozoa free in the lumen of the tubule on the 42nd day.


Spermatozoa were found in the efierent tubules on the 60th day, but may have been present there a few days earlier.


Degeneration occurs among some of the germ-cells in some tubules and many testes but no general wave of degeneration occurs at any time after birth, such as has been described in a number of mammals by various authors.


The time-relations of spermatogenesis described above coincide in a remarkable manner with those recorded by Allen (1918) in the albino rat. This author found primary spermatocytes appearing in the tubules on the 7th to 10th day. These reached the pachytene stage by the 14th day and simultaneously the lumen first appeared. He found the first crop of spermatozoa in the tubules on the 37th day. Hewer (1914), however, also Working on rats, obtained very different results, finding for the first time primary spermatocytes at 3% weeks, a lumen at 7 weeks, spermat-ids at 8 weeks, spermatozoa at 9 weeks and at 10 weeks a second crop of spermatozoa in the testis and the first crop in the epididymis. .A.llen’s results, although in marked contrast to Hewer’s, conform very closely to our results on the mouse. Moreover. he employed only rats of the standard strain of the Wistar Institute, and thus probably obtained reliable results. We employed also an inbred strain of mice, thus obtaining greater uniformity than would be possible with animals of different strains. We lay great stress on the importance of employing only such material for work on the testis, since this organ is very sensitive to the general condition of the animal. It would appear, therefore, that the time relations of the chief phases of spermatogenesis in the immature rat and mouse are remarkably similar and that in both mature spermatozoa are produced on or about the 40th day.


Allen points out that according to Dona.ldsou’s tables (1924) the testes of the rat weigh 0-067 gm. at 14 days old and 0-244 gm. at 37 days. Thus in the rat, the testes almost quadruple their weight from the time when pachytene nuclei are plentiful until the first crop of spermatozoa are produced. During the corresponding period in the mouse the weight of the testes increases from 12 :5; 4 mg. at 14 days to 120 :1; 20 mg. at 42 days, z'.e., by about 10 times their initial weight.


The male rat, according to Donaldson (1924), has a body weight of 38 gm. at 37 days and 280 gm. at 365 days when the curve is almost flat. Thus it may reach a body weight eight times as great as that when it first produced mature spermatozoa in the testis. The cleaned-body weight of the mouse is 13-5 i 2 gm. at B days and 27 :1; 5 gm. approximately at 300days-when the curve is flattening. Thus the mouse only doubles its weight subsequently to the appearance of mature spermatozoa in the testis. Taking the appearance of mature spermatozoa in the testis as a satisfactory criterion of puberty it is remarkable that whereas the mouse only doubles its weight subsequently, the rat can attain a weight eight times that at puberty. The mean weight at birth of a male rat is 4 -7 gm., according to Donaldson, while in the male mouse it is 1 -41 gm., as given by Parkes (1926) using the same strain of mice, for the mean birth weight of males and females combined, a weight which conforms well with our data. Robertson and Ray (1916) record a birth weight in 56 mice of 1-23 gm., which is rather lower, and Kopec (1930) records a birth weight for male mice of 1 -25 gm. It is apparent that the male rat attains a weight rather over eight times and the male mouse, taking Parkes’ figure of 1 -41 gm., rather over nine times its birth weight at puberty as judged by the presence of mature sperms in the testis. It is subsequent to puberty therefore that the notable difference in the growth of these two nearly related species occurs.


Reviewing the more salient points in the time relations of growth of the testis it is significant that the greatest increase in the diameter of the spermatic tubules, occurs at about a fortnight old, simultaneously with the appearance of the maximum number of spermatocyte nuclei in pachynema and of lumina in the tubules. The most rapid growth of the testes is taking place at 30 to 40 days, at the same time as the spermatic tubules constitute a maximum part of the testis, as shown by the relative area of intert-ubular to tubular tissueon age, fig. 9, and shortly before mature spermatozoa are produced. finally the percentage body weight of the testes reaches a. maximum at about 40 days at the time when the increase in the diameter ofthe spermatic tubules is ceasing, fig. 6, and when mature spermatozoa are produced, and the histological picture presented by the testis is that of a mature animal.

Summary

  1. Approximately 140 male mice, all taken from an in-bred colony, whose ages ranged from birth to upwards of 300 days, were employed in this research.
  2. The cleaned—body weight and the weight of the testes was obtained for each animal.
  3. The data for the growth on age of (a) cleaned-body weight, (b) weight of testes, (c) mean diameter of spermatic tubules, (d) area of spermatic tubules in transverse section, (e) area of intertubular tissue in transverse section, together with the growth of testes on cleaned-body weight, are given in the form of scatter diagrams. A linear regression has been fitted for the right testis on the left and it is shown that the right testis is significantly heavier than the left.
  4. The maximum number of primary spermatocyte nuclei in paehynema occurs on the 14th day, together with the appearance of a lumen in many of the spermatic cords, while at about the same time the increase in the mean diameter of the spermatic tubules attains a maximum and all the cords become luminate.
  5. Mature sperms appear first in the testis of the mouse on the 42nd day while in the rat they appear on the 37th day (Allen, 1918). The appearance of mature sperms in the testis provides an easily determined and clearly defined point in the period of puberty. From birth to puberty, so defined, the rat increases its body weight by eight times, the mouse by nine times. Afterwards whereas the rat attains a weight eight times that at puberty when it is a year old, the mouse only doubles its weight from puberty to about 300 days.
  6. The testes attain their maximum growth rate at 30 to 4:0 days, at the time when the area of spermatic tubules in a transverse section relative to the area of intertubular tissue is at a maximum.
  7. Although there is a greater tendency towards degeneration of a small percentage of germ-cells in some of the spermatic tubules, about the time when the majority of spermatocytes are in pachynema, no generalised wave of degeneration, such as has been described in some mammals, occurs between birth and maturity.


Bibliography

Agdhur (1927). Aota Zool., vol. 8.

Allen, E. (1918). J. Morph., vol. 31.

Brambell, F. W. Rogers (1927). Proc. Roy. Soc. B, vol. 101, p. 391.

Donaldson, H. H. (1924). The Rat, Philadelphia.

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Cite this page: Hill, M.A. (2024, March 19) Embryology Paper - Development of the Mouse Gonads 4. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Development_of_the_Mouse_Gonads_4

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