Adolescent Sterility in the Male Guinea Pig
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1 Adolescent Sterility in the Male Guinea Pig Richard C Webster, PhD, * and William C Young, PhD THE PERIOD of adolescent sterility as it is designated in the female primate is the interval of time which elapses between the first menstruation and the ability to conceive and carry a fetus to term2 It may perhaps be a period of anovulatory cycles as Hartman suggested, or it may be a period during which ovulation is occurring, but during which the functional activity of the corpus luteum is inadequate for the maintenance of pregnancy14 In either case it is a phase in the process of sexual maturation in the female The condition is not necessarily confined to primates A somewhat comparable state has been reported as occurring in the mouselo and the COWl2 As far as the writers have been able to ascertain, the possibility that there is a sterility or relative sterility of adolescence in the male has not been suggested, although the existence of such an interval might seem to be indicated by the observations of Lataste and Stone Lataste stated that his guinea pigs copulated at 2 months of age, but that fertilization was accomplished only after they were 2~ months old If Lataste did not confuse pre-ejaculatory intromission accompanied by pelvic thrusts with ejaculation, his observation that the first copulations usually are sterile certainly anticipated the point we will develop in this communication But it is now known from unpublished observationsl3 that intromissions with pelvic thrusts which are not accompanied by ejaculation have in the pastl been confused with ejaculation If Lataste made this excusable error, he may From the Department of Anatomy, University of Kansas, School of Medicine This investigation was supported in part by a research grant from the Division of Research Grants and Fellowships of the National Institutes of Health, U S Public Health Service Now Assistant Professor of Anatomy, Indiana University, School of Medicine 175
2 176 WEBSTER & YOUNG [Fertility & Sterility not properly be considered to have been the first to observe that the first ejaculations usually are sterile Stone's observation that in the rat the awakening of copulatory ability frequently precedes the development of full spermatogenic activity would seem to have anticipated our observation that the first ejaculations are usually sterile The possibility is excluded, however, by the circumstance that his definition of the copulatory act denoted the overt elements of the copulatory response without implications as to the delivery of spermatozoa into the female As far as we have been able to ascertain, therefore, from the literature dealing with the sexual maturation of the guinea pig and rat,3 4, 5 7, 8, 9, 11 unequivocal evidence that the first ejaculations usually are sterile has not been presented MATERIALS AND METHODS Data with respect to sexual maturation were obtained from 20 male guinea pigs of known age Each male was weaned when 20 to 25 days old and isolated in a single cage Mating tests with females in heat were begun between the twenty-second and fiftieth day of age and continued at intervals from one to thirteen days until the fertility of the matings was established Most of the 294 tests were made at intervals of from three to six days In order to obviate the difficulty of mating which might come from the use of large females with small males, females that were approximately the size of the males were used Their ages during the periods of sterile copulations varied from 54 days to 10 months Inasmuch as many young female guinea pigs become capable of reproduction as early as the fortieth to the forty-fifth day of age, and conception as early as the twenty-sixth day has been recorded,3 it is concluded that the age of the females used during the phase of sterile matings was well beyond that at which there would be any question with respect to their reproductive capacity The procedure employed in testing male guinea pigs for strength of drive is described elsewherey It is sufficient to say here that each test was of ten minutes' duration and the measures of behavior such as nibbling at the hair, nosing of the perineal region of the female (nuzzling), mounting, intromission without ejaculation, and ejaculation were recorded for each fifteensecond period of the test During the sexual maturation of a male these measures of behavior tend to appear in the order given
3 Vol 2, No2, 1951] MALE GUINEA PIG 177 ; With a little experience, intromission with ejaculation can easily be distinguished from intromission without ejaculation When ejaculation occurs the final pelvic thrust is conspicuously prolonged and there is a drawing in of the Hanks of the male as in a spasm Equally diagnostic when it follows the above described reaction, is an almost immediate dragging of the pudendum along the Hoor of the cage, very much as a dog infested with intestinal worms will do When ejaculation occurred the female was isolated and observed daily for from fifteen to twenty days, at which time it could be determined from the condition of the vaginal membrane whether or not impregnation had occurred Tests of each male were continued, however, until it was known that one copulation had been fertile The pregnant animals were kept under observation until the termination of pregnancy when the length of gestation and the size and condition of the litter were recorded After the tests had been completed, the age of the males at the time of the first intromission, the first ejaculation, and the first fertile ejaculation were determined A precise correlation of changes in behavior with the degree of spermatogenesis such as Stone made for the rat was not attempted This was not practicable because the first fertile mating could not be identified as such until fifteen to twenty days after it had occurred Instead, the epididymides of 19 males not used for the mating tests were examined for motile spermatozoa on the fiftieth, sixtieth, and eightieth day of age which, as we learned, is approximately the time of the first intromission, the first ejaculation, and the first fertile ejaculation, respectively OBSERVATIONS The data summarized in Table 1 are largely self-explanatory Except for two animals (215L and 465T), there were intervals varying from fourteen to forty-four days (mean, 307 days) between the first intromission with pelvic thrusts and the first fertile copulation If we accept the dictionary definition of copulation as a union of opposite sexes, this interval would be the period of adolescent sterility in the male In eight animals (189, 208L, 211L, 311, 341, 346, 360, and 461 T) this period could be divided into an interval between the first intromission and the first ejaculation which was sterile, and a second inte~val between this first sterile ejaculation and the first fertile ejaculation The length of the former interval varied from 4 to 38 days (mean, 151 days) The length of
4 178 WEBSTER & YOUNG [Fertility & Sterility the interval between the first sterile and the first fertile ejaculation also varied from 4 to 38 days, but the mean was 181 days In 7 animals (181, 21OT, 231T, 303, 456T, and 466T) the first ejaculation coincided with the first intromission, consequently all of the period of adolescent sterility was represented by the interval between the first sterile ejaculation and the first fertile ejaculation Its length varied from 18 to 41 days (mean, 287 days) In 3 animals (380L, 459L, and 464T) there were intervals from 14 to 38 TABLE 1 The Age of 20 Male Guinea Pigs at Sexual Maturation Age in Days at Age in Days at Age in Days at First Animal First Intromission First Eiaculation Fertile Copulation L T L T L T L T L T T T T Mean 535 ± 08 (PE) 639 ± 30 (PE) 811 ± 16 (PE) days between the first intromissions and the first ejaculations, but the latter were fertile In these animals, therefore, the interval during which there were intromissions without ejaculation constituted the period of adolescent sterility In the 15 animals in which there was an interval between the first sterile ejaculation and the first fertile ejaculation, its length varied from 4 to 41 days (mean, 23 days) During this interval, from one to six sterile ejaculations preceded the first fertile ejaculation
5 Vol 2, No2, 1951] MALE GUINEA PIG 179 The explanation for the sterility of the copulations during which there were pelvic thrusts but no ejaculation is obvious The sterility of the copulations during which ejaculation occurred presented somewhat more of a problem, but no great difficulty It was due apparently to a deficiency of spermatozoa in the ejaculates The epididymides of the seven males killed on the fiftieth day contained no spermatozoa On the sixtieth day a few motile spermatozoa were found, but in instances not more than two to a field were seen under low-power (40 X) magnification On the sixtieth day the epididymides were still not white By the eightieth day, in the 6 males that were examined at this time, the tails of the epididymides were white and well filled; suspensions of their contents teemed with spermatozoa in numbers comparable with those present in specimens from males of proved fertility The hypothesis that the frequent sterility of the first ejaculations of which a male is capable is attributable to a deficiency of spermatozoa, receives support from the data summarized in Table 1 It will be observed that the 5 males (215L, 380L, 459L, 464T, and 465T) in which the first ejaculation was fertile were 89 to 96 days old at the time of ejaculation It is presumed from the fertility of these matings and from the number of spermatozoa in the epididymides on the eightieth day, that spermatogenesis had proceeded at a normal rate, but that there was a lag in the development of some other attribute necessary for reproduction Stone concluded from his study of the rat that an immaturity of the penis or a retarded development of sex drive could account for the failure of many animals to achieve the ability to copulate Our records of the 5 guinea pigs in which the first ejaculation occurred so late indicate that a low sex drive rather than any immaturity of the penis was involved In 3 of the males (215L, 464T, and 465T) little behavior above nuzzling was ever attempted, and in 2 (380L and 459L) the capacity for intromission was achieved fairly early but sex drive remained generally low The observations confirm the hypothesis advanced by Stone that the development of spermatogenesis and the maturation of sex drive do not necessarily have a fixed relationship to each other Of the 20 pregnancies which followed the first fertile matings, 15 were terminated normally, 3 were terminated prematurely by abortion or resorption of the fetuses, and 2 were terminated by the death of the female from infections in the colony that were not related to pregnancy The course of
6 180 WEBSTER & YOUNG [Fertility & Sterility gestation, therefore, was not different following the first fertile copulation by -,0 these males than it was following copulations by older males in the colony DISCUSSION The observations described above would appear to be the first of their kind to be recorded Consequently, it is not known whether there is a period of adolescent sterility in males of other species We are indebted however to Alfred C Kinsey for unpublished information with respect to the human male In an exchange of correspondence Professor Kinsey has written as follows: "Unpublished data gathered by the group studying sex behavior at Indiana University indicate that there may be a period of some years of adolescent sterility in the human male The data confirm the previously published work on adolescent sterility in the human female and indicate something of the same sort for the human male We have a very few records of younger adolescent males being responsible for pregnancies even in groups where coitus is frequent and no form of contraception is employed Some data exist on the presence of spem1 in the first ejaculates of human males, but we are inclined to believe that sperm counts may be too low in the younger human male to effect fertilization We would emphasize that there must be considerable individual variation on all these matters" The information Kinsey has obtained enhances interest in the more precise data that can be accumulated during experiments on lower mammals SUMMARY During the sexual maturation of 18 of 20 male guinea pigs the first intromission with pelvic thrusts occurred at 535 ± 08 days of age, the first ejaculation which was sterile at 639 ± 30 days of age, and the first fertile ejaculation at days of age In only 2 animals which matured late, did the first intromission and the first fertile ejaculation coincide The interval between the first intromission and the first fertile copulation is designated as the period of adolescent sterility in the male The failure of ejaculation accounted for most of the sterility during the early part of the period, and a deficiency of spermatozoa in the ejaculate seems to have been responsible for the sterility later, during the period of sterile ejaculations In the guinea pig as in the rat, the development of
7 Vol 2, No2, MALE GUINEA PIG 181 spermatogenesis and the maturation of sex drive are not necessarily strictly correlated in time REFERENCES 1 Armitstead, R B: J Exper ZooI 41: , Ashley Montagu, M F: Adolescent Sterility Springfield, Illinois, Charles C Thomas, Avery, G T: J Compo PsychoI 5: , Beach, F A: J CHn EndocrinoI 4: , Beach, F A, and Holz, A M: J Exper ZooI 101:91-142, Hartman, C G: Science 74: , Henocque, A: Compt rend Soc de bioi, Ser 9, 2: , Lataste, F: Compt rend Soc de bioi, Ser 9, 4: , Louttit, C M: J Compo PsychoI 9: , Mirskaia, L, and Crew, F A E: J Exper BioI 7: , Stone, C P: Am J PhysioI 68: , Winters, L M, Green, W W, and Comstock, R E: University of Minnesota Agricultural Experiment Station, Technical Bulletin 151: Young, W C: J Compo & PhysioI PsychoI In press 14 Young, W C, and Yerkes, R M: Endocrinology 33: ,1943
(Received 5th July 1968)
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