Paper - A study of the function of the epididymis 1 (1929)
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Young WC. A study of the function of the epididymis. I. Is the attainment of full spermatozoon maturity attributable to some specific action of the epididymal secretion?. (1929) J Morphol. 47(2): 479-495.
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A study of the function of the epididymis
I. Is the attainment of full spermatozoon maturity attributable to some specific action of the epididymal secretion?
William C. Young
RiiU Zoological Laboratory, The University of Chicago
- This work was aided by a grant from the Committee on Sex Research of the National Research Council; grant administered by E. B. Lillie.
During the past few years many functions have been assigned to the epididymis which have been supplementary to its role in sperm storage and to its secretory activity. One of these, the suggestion that sperm attain full maturity and are strengthened in consequence of some action of its secretion, has been reinvestigated as the first part of a study which is intended to include other aspects of the problem.
No evidence in support of the theory was obtained from a series of experiments on various mammals representing a repetition and extension of earlier work. On the contrary, the .strengthening and attainment of full spermatozoon maturity would seem to be the outcome of changes which are inherent in the sperm themselves. It is suggested, therefore, until other aspects of the subject can be reinvestigated, that the epididymis is simply a reservoir for sperm in which the processes of sperm development which start while they are still contained in the testis are free to continue because of the favorable environment present in the epididymis.
The problem of the fiinetioii of the epididymis arose as the outcome of an investigation of the histological changes which occur in the guinea-pig testis follovwing the application of temperatures slightly higher than that of the body (Young, ’27). Since becoming interested in the problem, however, the opinions with respect to epididjnnal function have been found to be so numerous and the methods of investigation so varied, that it has seemed advisable to investigate its different aspects separately. The experiments reported in this paper represent a study of that phase of the problem which is related most closely to my earlier work cited above. The results from the investigation of other aspects of the problem will be reported as soon as they have been obtained.
In the earlier study (Young, ’27) water heated a few degrees above body temperature was allowed to run over the guinea-pig scrotum. At frequent intervals from one hour until one year after the treatment, testes were removed and studied histologically. The degenerative changes which were known to folloAv such a treatment (Moore, ’24) were found to occur in a definite order. The actively dividing primary and secondary spermatocytes and the younger spermatids were the first cells to show degenerative changes. The older spermatids were the next to he msibly affected and, subsequently, the degeneration of spermatozoa was observed, those in the epididjunis, hoAvever, being more resistant than those in the testis. Spermatogonia were among the most resistant germinal elements and many usually survived the heat injury to serve as the stem cells for a new germinal epithelium. It was shown, therefore, that male germ cells exhibit a rising and falling gradient of susceptibility to high temperature as they develop.
These observations might not have been commented upon further had it not been for a suggestion as to epididymal function advanced by Stigler (’18). He, too, had observed in the guinea-pig, rat, and mouse that sperm contained in the epididymis are more heat resistant than those in the testis. He stated, in addition, that those contained in the posterior end, of the epididymis are more heat resistant than those contained in the anterior end, and that sperm contained in the second and subsequent ejaculates of a series are less heat resistant than those contained in the first ejaculate. He concluded that sperm experience a strengthening -which increases their heat resistance and, presumably, resistance against other physiological factors as well.
His theory was referred to without comment (Young, ’27, p. 492), except for the suggestion that confirmatory experiments seemed desirable. Having pointed out that the heat resistance of male germ cells increases progressively following the comiiletion of the reduction divisions until they have attained their final form as spermafozoa, it seemed strange that some external factor such as epididymal action should have to be invoked to explain further increase in resistance during their residence in tliis organ. In fact, it seemed more probable that this progressive increase in re.sistance to high temperature is simply an expression of changes which are inherent in the germ cells.
An examination of the literature revealed no similar suggestion, except for a short statement made by von Mollendorff during the meeting of the Anatomischen Gesellsehaft in Halle in 1924 and referred to by Redenz (’24, S. 607). According to von Mollendorff, the changed properties of sperm which appear after they have passed through the epididjunis may depend on a change in the colloidal state of the sperm and on a transformation in their protoplasm, and not on the microscopically invisible covering which Redenz has postulated to exist as a product of the epiclidjunal secretion. Much evidence, on the other hand, seemed to oppose this idea and that expressed by myself, and to support Stigler’s theory that the strengthening of sperm during their residence in the epididymis is attributable to some action of the epididymal secretion.
Most important, perhaps, were the observations that sperm removed from the posterior levels of the epididjmis and placed in physiological saline solution show a stronger movement than those removed from the anterior levels and testis (Hammar, ’97; Walker, ’99; Tournade and Regaud, ’ll; Tournade, ’13, and Mettenleiter, ’25). Of this group, Touriiade actually attributes tlie stronger motion of sperm from the posterior levels of the epididymis to some action of the secretion of this organ — a conclusion with which von Lanz (’24 a and b) agrees. Other observations which have been quoted in support of this theory of epididymis function were those to the effect that the second and subsequent ejaculates in a series contain fewer and less active sperm than the first (Mantegazza, ’66, for man; Lewis, ’ll, for horses; LloydJones and Hays, ’18, for rabbits; and Amantea and Krzyszkowsky, ’21, and Krzyszkowsky and Pawlow, ’27, for dogs).
The problem as outlined has been studied during the past months, and the results and conclusions are repoi’ted below. I am indebted to Prof. Prank K. Lillie for his assistance in making the study possible and to Prof. Carl R. Moore for his counsel and help during the progress of the work.
a. The motility of sperm from the seminiferous tubules
Probably the most important evidence for the conclusion that spermatozoa attain their full maturity in consequence of some action of the epididymal secretion was the observation noted above, that sperm removed from the testis and anterior end of the epididymis are non-motile when placed in physiological saline solution, while those removed from the posterior levels are motile (Hammar, ’97, for the dog; Tournade and Eegaud, ’ll, for the rat; and Tournade, ’13, for the rat, rabbit, guinea-pig, and dog). It seemed desirable to reinvestigate this point.
Sperm from the seminiferous tubules of three bulls, five rams, four guinea-pigs, and four rats were examined folloiving the maceration of small fragments of the testis in Locke’s solution. In the bull, guinea-pig, and ram some sperm from each testis were observed to exhibit a weak but nevertheless distinct vibratile movement of the tail. In the rat many sperm were found to be motile, a strong progressive motion being shown. These observations do not agree with those of Hammar, Tournade, and Eegaud, but they are consistent with those reported by Walker (’99), who found that sperm from the testis of the dog can be activated slightly by the addition of prostatic secretion.
Sperm from the head, body, and tail of the epidkhmiis of the bull, ram, and rat were examined nest. The impression is gained that motion is strongest in the tail and weakest in the head — observations which are in agreement with those of Hammar, Tournade and Regaud, and Walker. The point should be confirmed, however, by more precise methods than have been used thus far.
It is seen, then, that although the capacity for motion appears to become strengthened as sperm pass through the epididjTuis, that its first appearance can be observed while the sperm are still contained in the testis. The oliservation is. interpreted as indicating that the acquisition and strengthening of motility is not attributable to any specific action of the epididymal secretion, but is an expression of sperm development, the capacity for which is inherent in the spermatozoon itself.
b. The resistance of sperm from different levels of the epididymis to high temperature
In the second group of experiments directed toward an investigation of the theory that spermatozoa attain their full maturity in consequence of some action of the epididjunal secretion, a study of the heat resistance of sperm from different parts of the epididymis was made. It vnll be recalled that Stigler heated sperm removed from the testis and epididymis as well as sperm obtained from successive ejaculates and found, in the first case, that those from the testis are less heat resistant than those from the epididymis, and, in the second case, that sperm from the second and subsequent ejaculates are less resistant than those from the first. To the writer it seemed justifiable and fully as accurate to remove sperm from the proximal and distal ends of the epididymis, place them in Locke’s solution in as nearly equal concentration as possible, subject them to a given simultaneous temperature exposure in a water-bath, and observe the moment when motion is no longer visible on the part of any one sperm. A temperature of 46'^ C. was chosen after some preliminary, trials.
Spermatozoa were removed from twenty-five guinea-pigs and studied in this manner. The data from ten typical experiments are shown in chart 1.
Animal Wo. 2 .
Chart I - Heat restsiance of sperm froni proximal and . distal ends of epididysTnis tail (guinea pig).
CO 7e mins.
85 mins. 55 mins.
10 mi ns. sg mins.
30 70(715. a SSTnms.
Proximail end Distal end
_ 105 TDITIS, 100 mins.
The result was that, contrary to what was expected on the basis of Stigler’s work, spei*m from the proximal end of the epiclicljTnis were found to be more resistant when exposed to high temperature than sperm from the distal end. The average limit of motion of sperm from the proximal end, compiled from the records of twenty-five guinea-pigs, was 105 minutes, Avhile the average limit of motion of sperm from the distal ends of the epididymides was only 76 minutes. Sperm from the proximal end were conspicuously more heat resistant in fifteen eases, there was but little difference in six cases, and sperm from tlie distal end were slightly more heat resistant than those from the proximal end in four cases.
The unexpected result suggested a repetition of the experiment using sperm from other species, and the rat and ram were selected. Both provide better material for such an experiment than the guinea-pig. The head, body, and tail of the epididymis are sharply divided in both species, and, in the rat, sperm from the testis are so motile when placed in Locke’s solution that they, too, can be compared with sperm from the two parts of the epididymis. The data for sperm from the testis, epididymis head, and epididymis tail of five rats are shown in chart 2.
Animai Mo. I:
Chari H - Hedt resistance of sperm froTn the testis,, epididymis head, and epididymis tail (ra!).
- 75 mins.
4Z mi ns, 47 mins.
85 Tnins. 8p mi ns.
The agreement with the results obtained when guinea-pig sperm were used is perfect. Sperm from the epidid^unis head were motile for as long as eighty-three minutes, averaged for the five animals, while those from the epidid^unis tail were motile for only seventy minutes. Sperm from the epididymis tail were more heat resistant than those from the epididymis head in only one out of five cases. Sperm from the testis were the least heat resistant, the average limit of motion being only forty-four minutes.
The data obtained from eight rams when sperm from the epididymis head, body, and tail were heated separately axe shown in chart 3.
Results which are consistent with those obtained previously by myself on the g’uinea-pig and rat and contradictory to those reported by Stigler were obtained. The average limit of motion on the part of sperm from the epididymis head was 107 minutes, on the part of sperm from the epididymis body it was 122 minutes, and on the part of sperm from the epididrunis tail it was only 78 minutes. In the ram, sperm from the tail, located distally, were found to be less resistant than those from the proximally located body in every animal.
Chart IE - Heat resistance of sperin from the- epididymis head, body, and tail (ram).
6 0 Tn i n 5,
• 120 mi ns. 115 mins.
bo Tnins. bO mins.
= !30 mins.
- - - — 145 mins.
— (40 mins.
. , r, , loo Tnins.
- - 1(5 mins.
-- no mins.
and less resistant than those from the epididymis head in seven out of eight animals.
This apparently satisfactory demonstration that sperm from the anterior portion of the epididymis of the guinea-pig, rat, and ram are more resistant when exposed to high temperature than sperm from the posterior portions of the same epididjunides raised the following question: How are data from these experiments in which sperm from two ends of the epididj-mides w-ere heated directly to he reconciled with the results obtained by Stigler, who heated sperm from successive ejaculates?
Final answer to the question must await the opportunity to repeat in every detail the procedure followed by Stigler. In the meantime, however, it is thought that observations which have been reported by other investigators may suggest the answer. The work of Mantegazza (’66), Lewis (’ll), LloydJones and Hays -(’18), Amantea and Krzyszkowsky (’21), and Krzyszkowsky and Pawlow (’27), in which attention is called to the reduction in the number of sperm contained in successive ejaculates, has been cited. It seems likely from this that the number of sperm in the second ejaculate may have been less than the number in the first ejaculate in the experiment performed by Stigler. Simultaneously, the idea Tvas suggested that the greater dilution of sperm in the second ejaculate may be a factor of some importance. Barthelemy (’26) has shown that the dui’ation of motion of frog sperm is longer when the concentration of sperm is increased, and Gray (’28) has shown that Echinus sperm live longer in concentrated suspensions than they do in dilute suspensions.
A simple experiment was arranged to test the point for the guinea-pig. Epididymides were macerated in about 25 cc. of Locke’s solution and the sperm suspension poured off. This suspension was considered to be full strength and various dilutions were made by adding one or more parts of Locke’s solution to a constant volume of sperm suspension. In this way dilutions of 1/2, 1/3, 1/4, 1/7, 1/8, 1/14, and 1/25 -were obtained. Test-tube samples were then heated in a waterbath at 46 °C., and the time recorded when the last motile sperm was observed. The results are shown in table 1.
The decrease in resistance to high temperature with increased dilution is clearly demonstrated for guinea-pig sperm. Of course, it cannot be known that a greater dilution of sperm in the second ejaculate than in the first will likevuse explain the decreased heat resistance of sperm contained in the second and subsequent ejaculates until Stigler ’s experiments can be repeated. In the meantime, however, it is difficult to account for the lower resistance of the sperm contained in the second ejaculate in any other way, when it has been demonstrated on so many animals that sperm in the distal end of the epididymis are generally less heat resistant than those from the proximal end.
The significance of this group of experiments for the problem of the function of the epididymis may be summarized as follows :
1. Spermatozoa removed from the distal portion of the epididymis have been found to be less heat resistant than those removed from the proximal portion. The theory, therefore, that spermatozoa become progressively more heat resistant as they pass through the entire length of the epididymis should be abandoned.
lEifcct of dilution on dumtion of motio7i of guinea-pig sperm mamtained at 46° C.
PARTS OP LOCKE’S SOLUTION" TO UNDILUTED SPERM SUSPENSION
2. There is some increase in heat resistance as sperm pass through the proximal portion of the epididymis lumen; at least this is true in the ram, wdiere sperm from the body have been shown to be more heat resistant than those from the head. It has been shown, however (Young, ’27), that this change in heat resistance begins while the germ cells are still contained in the testis and, in addition, in this study, that the increase in heat resistance is not continued as sperm pass through the body into the tail. On the contrary, sperm contained in the tail are less heat resistant than those in either the body or head. For these reasons, therefore, changes in heat resistance which do occur in sperm during their residence in tke epididymis pi’obably should be conceived as being independent of any specific action by its secretion.
3. It is suggested that the lower resistance of sperm from the second and subsequent ejaculates of a series to high temperature, as reported by Stigler, may be attributable to a greater dilution of sperm in these ejaculates than in the first, rather than to the immaturity of the sperm.
Chart E " Resistance of sperm from proximal and distal ends of epididymis tail to ultraviolet radiation (guinea pig),
- 45 mins.
f. fST mins.
— 33 mins.
2. 33 mins.
» 45 mins, Proximal end
3. 25 mins. Distal end
— . 30 mins.
4. r.LLM n 13 mins.,
5. c ,- . mm 15 mins.
mini III IT mi n s.
b. r rn i i i. i 17 TTlinS.
- 30 mins.
I c x3T r - i r .i (5 mins.
c. The resistance of sperm from different levels of the epididymis to ultraviolet radiation
A third series of experiments, arranged for the piirpowse of reinvestigating the theory that the strengthening of sperm as they pass through the epididymis is attributable to some specific action by the epididymal secretion, was similar to the second series, except that sperm from dilferent levels of the guinea-pig epididymis were exposed to ultraviolet radiation instead of to high temperature. Unscreened radiation from a quartz mercury-vapor arc running at 110 volts, D.C., at 41 amperes was employed. Exposures were made at a distance of 44 cm. from the center of the arc. The results are shoAvn in chart 4.
Except for tlie much shorter duration of motion on the part of all sperm, the results are no different from those obtained ■when sperm were exposed to high temperature. In six out of eight eases sperm from the proximal end were more resistant than those from the distal end, in two cases no difference was observed, and sperm from the distal end were not more resistant than those from the proximal end in a single experiment. The average limit of motion by sperm from the proximal end of the epididymis ivas thirty-three minutes, while those from the distal end remained motile for an average of only nineteen minutes.
Stigler’s suggestion, therefore, that sperm resistance against other physiological factors as well as high temperature increases as they pass through the epididymis has not been confirmed by the employment of ultraviolet rays.
The experiments which have been described represent an effort to solve one of the problems involved in a study of the function of the epididymis. Several workers, but particularly Stigler, and Tournade and Regaud, have accepted observations of a diverse nature as evidence for the conclusion that the secretion of the epididymis exerts a strengthening action on spermatozoa which is manifested by a stronger capacity for motion and by an increased resistance against high temperature and other physiological factors as well. . Many of the experiments from which this suggestion followed have been repeated and supplemented, but no evidence has been obtained which can be regarded as confirming the conclusions of these earlier investigators.
For example, Hammar, and Tournade and Regaud state that sperm are non-motile in the testis and anterior levels of the epididymis, but strongly motile in the posterior levels
from which it has been concluded that sperm acquire their capacity for motion as they pass through the epididymis and as a result of some action of its secretion. My own observations on four species and sixteen individuals indicate that sperm’s capacity for motion becomes strengthened as they pass through the epididymis, but also that many sperm acquire their capacity for motion -while they are still contained in the testis. From this it is concluded that at least one manifestation of sperm strength, namely, the capacity for motion, is acquired independently of any specific action of the epididymal secretion.
Stigler has cited experimental evidence in support of the statement that siDennatozoa contained in the distal end of the epididymis remain motile longer when exposed to high temperature than those from the proximal end of this organ. From this he concluded that the epididymal secretion exeids a strengthening influence on sperm Avhich increases their resistance against high temperature and presumably against other physiological factors as well. The observations of Hammar, and Tournade and Eegaud, described above, have been quoted in support of his suggestion and, in addition, the observations of Mantegazza, Levds, Lloyd- Jones and Hays, Amantea and Ivrzyszkowsky, and Krzyszkowsky and Pawlow, who have reported that sperm in the second and subsequent ejaculates of a series remain motile for a shorter time than those contained in the first ejaculate.
When the experiments arranged for a reinvestigation of this work had been completed, it was found that sperm from the distal end of the epididymides from forty-nine animals of three species were actually less heat resistant than those from the proximal ends. Like-wdse, when sperm were removed from the epididymides of eight guinea-pigs and exposed to continuous ultraviolet radiation, the same situation prevailed," sperm from the distal end became non-motile sooner than those from the proximal end.
The results ceidainly do not provide a demonstration that the secretion of the epididymis exerts a strengthening influence on spei-m as suggested by Stigler. They do suggest, however, either that sperm are not constantly strengthened as they pass through the epididymis or that resistance to high temperature and ultraviolet radiation are not necessarily expressions of sperm strengtli. Tlie first possibility is not consistent \ntli the observation that the capacity for motion, considered generally to be an expression of sperm strength, seems to become stronger as sperm pass through the epididymis. Furthermore, it would lead to the awkward conclusion that sperm in the middle of the epididymis are stronger than those about to be discharged. The second possibility, on the other hand, that resistance to high temperature and ultraviolet radiation are not necessarily expressions of sperm strength seems more probable and is the conclusion I have reached. There is nothing which discredits this suggestion in any of the experiments which have been reported. In addition, a strengthening in the sense of an increased capacity for motion may well be more important in the attainment of the egg than a strengthening in the sense of an increased resistance against high temperature and ultraviolet radiation.
The idea that it is capacity for motion which is a measure of sperm strength rather than resistance against high temperature suggests an explanation for the lower resistance of sperm removed from the distal end of the epididymis to both high temperature and ultraviolet radiation. It may be that the more active sperm found in the distal end are more susceptible to the destructive action of these two agents than the less active cells from the proximal end.
Less attention has been given to the observations of Mantegazza, Lewis, and the others on the lower number and vitality of sperm contained in the second and subsequent ejaculates of a series — ^from which it likewise has been concluded that the epididymis exerts a strengthening influence on sperm — than on the observations of Stigler. The importance of sperm density in any study of sperm vitality has been pointed out, however, and it would seem well, on this account, to withhold any eoncliision as to epididjunal function which is based on the vitality of sperm from successive ejaculates until the factor of sperm density has received further attention.
In the discussion of the experiments which have led to the conclusion that the epididymal secretion exerts no specific action on the strengthening of sperm as they pass through it, there has been no minimization of the importance of the epididymal secretion as a medium in which sperm are preserved during the maturing or ripening process which continues after they have been carried out of the testis. Attention has simply been directed to recently accumulated evidence against the theory that the stimulus which induces these maturing or ripening changes in sperm originates in the epididymis. When the capacity for motion is regarded as an expression of sperm strength, any action of the epididymal secretion in strengthening the capacity for motion is felt to be excluded by the fact that the capacity for motion may be gained before the sperm leave the testis. For those who have considered heat resistance of sperm to be a manifestation of sperm strength, any action of the epididymal secretion in strengthening sperm is felt to be excluded, 1) by the fact that the heat resistance of germ cells begins to increase before they have left the testis, and, 2) by the fact that spermatozoa in the distal end of the epididymis are generally less heat resistant than those in the proximal portion.
A last point for discussion concerns the present status of the problem. As was stated in the beginning, the experiments reported in this paper were directed toy^ard the solution of only one of the questions involved in a study of the function of the epididymis. Until the other aspects of the problem can be investigated, only a tentative hypothesis of the relationship between the epididjunis and the spermatozoa contained in it can be given. It is reemphasized that the epididjunis is essentially a reservoir for sperm. In it the processes of sperm development which started while they were still attached to the germinal epithelimn are free to continue by reason of the suitable environment present in the organ. It has not been demonstrated that the epididymis produces any substance which induces these changes.
1. Attempts to confirm the suggestion that spermatozoa attain their full maturity and are strengthened in consequence of some action of the epididymal secretion have been unsuccessful. On the contrary, evidence obtained from recent experiments indicates that the strengthening of sperm begins before they leave the testis and continues after they have been carried into the epididymis, but independently of any specific action of its secretion.
2. This theory does not minimize the importance of the epididymal secretion as a medium in which sperm are preserved during the maturing or ripening process. It would simply exclude the theory that the stimulus which induces ripening changes originates in the epididymis.
3. Until more attention has been devoted to the problem of the function of the epididymis, a tentative and probably incomplete hypothesis of the relationship between the epididymis and its contents, the spermatozoa, is given. It is reemphasized that the epididymis is essentially a reservoir for sperm. In it the processes of sperm development which start while the sperm are still a part of the germinal epithelium are free to continue because of the favorable environment present in the organ.
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