1. The middle and caudal third of the ampulla tubae are the regions where most of the eggs of Mesocricetus auratus Waterhouse are fertilized.

  2. The earliest fertilization resulting from evening matings prior to ovulation (assuming the ovulation peak to be at 3 a.m.) were obtained at 2 hours after ovulation. When copulation occurred the morning after ovulation, fertilized ova were not obtained at 2 hours after mating, but they were at 4 hours.

  3. The time of fertilization is most frequently between the 2nd and 10th hour after ovulation. About 91 per cent, of the eggs are fertilized during this period.

  4. On the basis of existing data it is not possible to speak of a family-specific or even an order-specific fertilization site for the mammalian egg.

There is little precise information in the literature as to the exact place where the union of the male and female gametes occurs in the genital tract of mammals. Yet it seems that an exact knowledge of the place of fertilization might be of great significance, not only for our understanding of the process of fertilization itself, but in its relation to the manifold problems associated with the limited span of time during which the capacity for fertilization persists in the sperm and egg, and to the physiology of later development and implantation.

In most writings about the early development of Man and other mammals, it is assumed that the egg is fertilized in the cephalic part of the oviduct. However, there is still insufficient evidence to justify such general assumptions. It would not be surprising if it should be shown that different species have different topographical positions of the fertilization site correlated for instance with such factors as spontaneous versus induced ovulation.

Such an unsatisfactory situation suggests the necessity of a review of our knowledge concerning the site of fertilization of the mammalian egg, and motivated me to investigate this problem.

This first study is based on the examination of 780 fertilized and unfertilized eggs from 66 golden hamsters, Mesocricetus auratus Waterhouse. The hamster was chosen because of its exact adherence to an easily determined sexual cycle. It ovulates spontaneously every 4 days in the early morning hours between 1 and 4 o’clock of the second day of the estrous cycle (Ward, 1946; Boyer, 1953). The ova are discharged at any stage from ‘first anaphase’ to ‘first polar body, second metaphase’ (Ward, 1948a). The animals used in this investigation were selected on the basis of simple daily vaginal inspection using the data of Ward (1946). This method has proved to be without failure.

Instead of the copulation and ovulation age of most authors (Graves, 1945; Venable, 1946; Boyer, 1953), I started my experiments using the developmental age of the fertilized ova as defined by Ward (1948b) but subsequently changed to a more realistic time scale, based on a revised estimate of ovulation time, as a result of observations to be given later. Developmental age is the time span from the earliest possible fertilization time of an egg until its immersion in fixative. The developmental ages included in my series were 2, 3,4, 5, 6,12, 18, 24, and 30 hours according to Ward’s data on ovulation time. For each age half of the animals had short periods for copulation in the evening (8.00-8.30 p.m.) before ovulation. The other half had a half-hour period for copulation in the morning about 7 a.m. after ovulation. Since Ward assumes the time of ovulation is 1 a.m., the developmental age and ovulation age would correspond in animals mated in the evening; in the animals mated in the morning the developmental age would be 6 hours less than the ovulation age. Unmated animals killed at the same time as these experimental series formed controls.

The entire genital organs were fixed immediately after death in Bouin’s fluid. The ovaries with the oviducts and connecting parts were embedded in paraffin from cyclohexanon, sectioned at 8 μ, and stained with iron hematoxylin (Weigert) without counterstain.

The tortuous pattern of the uterine tubes of the golden hamster made it extraordinarily difficult to establish the exact position of the tubal eggs. Therefore it was necessary to draw the whole oviduct section by section after cutting, recording the relative position of the female gametes or zygotes. At the same time histological differences in the construction of the wall of various levels of the oviduct were noted.

The hamster ovary is, as in many rodents, completely enclosed by an ovarial sac which is continuous with the infundibulum of the oviduct (Text-fig. 1). The length of the infundibulum is about 0·2 mm. The transition from the smooth bursa wall to the funnel is characterized by the appearance of relatively high and slender mucous folds or fimbriae which contain only a very delicate connective tissue framework. The infundibulum leads into the ampulla, which is about 1·2 mm. long. Its wall is thin, relatively non-muscular, and contains low, widebased mucosal ridges at rather regular intervals. Toward the isthmus the ampulla wall gradually increases in thickness, so that a sharp boundary between these tWO portions does not exist. It proved useful to designate a transitional section, about 0·6 mm. in length, between the ampulla and isthmus. The isthmus (approximately 1·7 mm. long) has a markedly narrower lumen than the preceding section of the oviduct, and carries numerous thick epithelial ridges which when cut perpendicularly appear somewhat club-shaped. In the transition from the isthmus to the uterine horn the number of ridges decreases, and they become lower. The lumen here becomes indented by small separate protrusions. In the tunica propria glands appear; these increase in number and dimension and mark the beginning of the uterus. In addition, a valve occurs at the tubal-uterine junction. In brief the oviduct of the hamster corresponds in structure and histology with that of the mouse as given by Sobotta (1895).

Fig. 1.

Schematic drawing of the oviduct and ovary in Mesocricetus auratus Waterhouse. The various segments of the oviduct are differentiated by the different contours of the lumen.

Fig. 1.

Schematic drawing of the oviduct and ovary in Mesocricetus auratus Waterhouse. The various segments of the oviduct are differentiated by the different contours of the lumen.

In Tables 1 (experimentais, mated) and 2 (controls, unmated) the distribution of 780 eggs in relation to their assumed ovulation age is presented. The eggs classed as ‘missing’ include both those for which a safe evaluation of their condition was not possible, and eggs which could not be found but which must have existed since there were more ruptured follicles or corpora lutea than recovered eggs.

Table 1.

Distribution and condition of the eggs from the mated animals according to hypothetical ovulation age (ovulation assumed at 3 a.m.) and time of mating

Distribution and condition of the eggs from the mated animals according to hypothetical ovulation age (ovulation assumed at 3 a.m.) and time of mating
Distribution and condition of the eggs from the mated animals according to hypothetical ovulation age (ovulation assumed at 3 a.m.) and time of mating
Table 2.

Distribution of the ova in the control (unmated) animals, grouped according to ovulation age to correspond with the experimental (mated) animals

Distribution of the ova in the control (unmated) animals, grouped according to ovulation age to correspond with the experimental (mated) animals
Distribution of the ova in the control (unmated) animals, grouped according to ovulation age to correspond with the experimental (mated) animals

Tables 1 and 2 permit an estimate of the number of ova which must have been produced from polyovular follicles. For the total number of 780 eggs there were 739 corpora lutea and 34 ripe follicles, so that there were 7 more eggs than follicles, either unruptured or luteinized. In other words 0·95 per cent, of the ova seem to have been derived from polyovular follicles.

The planning of the experiment was based on the assumption that ovulation occurs in the Syrian hamster at approximately 1 a.m. (Ward, 1946, 1948b). In my observations, however, at 3 a.m. 34 ripe eggs out of 49 mature ova (Tables 1 and 2) had not yet left their follicles. A few ripe follicles may persist, or degenerate through luteinization or atresia; their number is small compared to the number of expelled eggs. We also know that in an animal such as Meso-cricetus where a great number of eggs are expelled we should not expect all ripe follicles to rupture, as a small percentage may become atretic very late in development, just before rupture.

Ovulation takes place at a somewhat later time than that given by Ward. Her statement is based on 8 ovaries of 8 animals killed between midnight and 1.15 a.m. Only one of 13 ripe follicles had ruptured at midnight. In the short timeinterval from 12.30 to 12.45 a.m. Ward (1946) found three ruptured follicles, one in the process of rupturing, and 9 unruptured follicles. Half an hour later (1.00 and 1.15 a.m.) 7 follicles had ruptured, 6 follicles were just rupturing, and 9 were unruptured. In my females killed at 3 a.m. only 15 out of 49 ripe follicles had ruptured. According to Ward’s findings (48 follicles) and my data (49 follicles) only 33 out of 97 mature follicles had ruptured between midnight and 3 a.m. At 4 and 5 a.m. there were no more follicles ready for rupturing. All the Graafian follicles at that time showed early signs of atresia. So it seems doubtful whether the high point of ovulation actually lies at 1 a.m.: it seems rather to be an hour or two later. It appears on a basis of 109 ripe or freshly ruptured follicles that the peak of follicular rupture occurs between 1 and 4 a.m., i.e. on the average at 2–3 a.m. This corresponds to the ovulation time of the mouse (Snell, 1941). All the following time data are based on an assumed ovulation time of 3 a.m.

The main data of the results are given in Tables 16. A few minor points, however, which cannot be obtained from the tables, are dealt with in the text.

At 3 a.m. 11 of 14 ovulated eggs (combining the mated and unmated groups) were found in the beginning part of the ampulla (Tables 3 and 4), and only three lay in the periovarial space.

Table 3.

Age and distribution of eggs in the various segments of the oviduct in the mated animals. The numbers in parentheses are the numbers of fertilized eggs. In column one, m and e mean morning and evening mating respectively

Age and distribution of eggs in the various segments of the oviduct in the mated animals. The numbers in parentheses are the numbers of fertilized eggs. In column one, m and e mean morning and evening mating respectively
Age and distribution of eggs in the various segments of the oviduct in the mated animals. The numbers in parentheses are the numbers of fertilized eggs. In column one, m and e mean morning and evening mating respectively
Table 4.

Age and distribution of eggs in the various segments of the oviduct in the unmated controls, grouped according to ovulation age to correspond with the experimental (mated) animals

Age and distribution of eggs in the various segments of the oviduct in the unmated controls, grouped according to ovulation age to correspond with the experimental (mated) animals
Age and distribution of eggs in the various segments of the oviduct in the unmated controls, grouped according to ovulation age to correspond with the experimental (mated) animals

Two hours after the assumed time of ovulation, 55 of 58 eggs were found in the ampulla (Tables 3 and 4), while 3 eggs still remained in the infundibulum. One of these ova in which the head of a sperm was visible was in the metaphase of the second maturation division. Since eggs were not found in the infundibulum at a later time, it is concluded that the ova quickly pass the periovarial space and the infundibulum. Approximately 3 hours after ovulation all eggs should have reached the ampulla through which they slowly pass during the next 10-12 hours. The schematic diagram (Text-fig. 1) shows, along with the tortuous nature of the tube, the eggs on their journey through the oviduct, where in the case of a mating they are fertilized.

Table 3 shows that the first fertilized eggs are found 2 hours after the supposed 3 a.m. ovulation; sperm had then penetrated into 5 of 35 ovulated ova. Three of these 5 zygotes lay in the middle part of the ampullar region, while one egg was already fertilized in the cranial portion and another in the infundibulum.

One, 2, and 3 hours after estimated ovulation time 63 unfertilized and 17 fertilized eggs were in the ampulla compared to 3 ova only in the infundibulum. By 4 hours ovulation age the number of unfertilized ova diminishes rapidly. Therefore we can assume that fertilization in the infundibulum is the exception rather than the rule. Eight hours after estimated ovulation time 7 of 31 eggs were fertilized, or just in the process of fertilization; the spermatozoa had partially pierced the membrana pellucida in some, while in others they were in the act of penetrating into the gamete, or had just penetrated. The 7 zygotes lay in the slightly dilated mid- and caudal region of the ampulla (Tables 5 and 6).

Table 5.

Distribution of the early developmental stages of the golden hamster according to ovulation age. In column one, m and e mean morning and evening mating respectively

Distribution of the early developmental stages of the golden hamster according to ovulation age. In column one, m and e mean morning and evening mating respectively
Distribution of the early developmental stages of the golden hamster according to ovulation age. In column one, m and e mean morning and evening mating respectively
Table 6.

Distribution of zygotes in relation to the different parts of the oviduct

Distribution of zygotes in relation to the different parts of the oviduct
Distribution of zygotes in relation to the different parts of the oviduct

Some of the eggs with an estimated ovulation age of 3 hours (Tables 3 and 5) were in the process of fertilization. The head of the sperm was partly transformed into the male pronucleus. The haploid egg nuclei were in the anaphase or telophase of the second meiosis. If the mating occurred 4 or even 6 hours after the presumed ovulation time then 24 out of 31 fertilized eggs with an ovulation age of 10–12 hours had reached the pronucleus stage; in only one egg had the sperm penetrated shortly before death (Table 5). This egg, moreover, was the only one of this extensive material that was still in the beginning phase of fertilization 10 hours after the estimated time of ovulation, and 6 hours after copulation.

With an estimated ovulation age of about 16 hours, copulation having preceded ovulation by about 8 hours, 6 of 14 zygotes in the transitional region still possessed both pronuclei, in 6 others the first cleavage had occurred, and 2 were in the two-cell stage. The 9 eggs lying in the isthmus were in the pronucleus stage (Tables 3 and 5).

Only one embryo with an estimated ovulation age of 22 hours, copulation having occurred about 4 hours after ovulation as a result of a morning mating, lay in the transitional region in the two-cell stage; the remaining eggs had reached the isthmus.

Twenty-two hours following the estimated time of ovulation, in animals mated the evening before, 12 of 21 embryos in the isthmus had already developed to the two-cell stage, while 4 in the transitional region and 4 in the isthmus showed pronuclei; in one the nuclei were in synapsis.

With an ovulation age of 28-30 hours, after a morning copulation, in 6 of the zygotes in the transitional area the first cleavage was occurring while one embryo was at the two-cell stage. In the isthmus 9 eggs were in the pronucleus stage, 9 in the first cleavage stage, and 12 two-cell stages, while 2 eggs were still in the second maturation division (Table 5).

With an assumed ovulation age of 34-36 hours, copulation having followed about 4 hours after ovulation (Table 3), 4 zygotes in the transitional region were at the first cleavage stage. Of the 28 fertilized eggs lying in the isthmus only 2 zygotes were in the pronucleus stage. In one egg there was first cleavage, and 25 embryos were in the two-cell stage; one straggler still in the second meiosis lay in the lower ampulla (Table 5).

It is hardly probable that in every case all eggs ovulated (12 per animal) will be fertilized. According to the data it appears that in at most 4 of 38 animals all ovulated eggs were fertilized (Table 1). Twelve or more hours following ovulation 91 per cent, of the eggs ovulated were fertilized, and this may be expected to approximate the maximum for the golden hamster, about 9 per cent, of the eggs shed remaining unfertilized. Among 440 ova, 10 hours following the estimated time of ovulation and 6 hours after copulation, the beginning of fertilization was observed in only one case. From this I conclude that at an increased ovulation age no further fertilization occurs, despite the presence of sperm.

The earliest fertilization of the hamster egg in vivo therefore occurs at an ovulation age of 2 hours, while the ability to be fertilized decreases rapidly at about 10 hours after follicular rupture. The optimum time for fertilization for the hamster egg is therefore limited within the range from 2 to 10 hours after ovulation. During this interval the egg stays in the ampulla. It appears that no other place than the ampulla can reasonably be considered as a fertilization site; recently fertilized eggs in variable numbers were found in the middle as well as in the lower region of the ampulla.

The eggs obviously passed through the cranial portion of the ampulla in a short time. Thus at 3 a.m. 9 eggs lay in the beginning portion of the ampulla, while 2 had already appeared in the mid-ampullar region. Two hours later 49 eggs—among them one fertilized—were found in the cranial third of the ampulla, and 6 in the middle third. Two hours later still, that is at an estimated ovulation age of 4 hours, no eggs were found in the cranial ampullar segment. Almost all of the eggs lay in the slightly dilated middle third, while a few had reached the caudal section. From this it is clear that until the peak of fertilization time is reached, between 4 and 12 hours after ovulation, the egg will be found in the mid- and caudal third of the ampulla. There they seem to be in the most favourable position for fertilization, for only one early fertilization stage lies in the cranial third of the ampulla (Table 6). It may be concluded therefore that the union of the egg and sperm in the golden hamster takes place as a rule in the middle and lower third of the ampulla. Nevertheless, fertilization can occasionally occur in the cranial end of the ampulla as well as in the infundibulum.

According to my observations that fertilization of the golden hamster egg occurs chiefly in the middle and caudal third of the ampulla, the problem remains as to how far the morning mating (4 hours after ovulation) possibly influences the position of the fertilization site. At the time of the morning copulation (7 a.m.) practically all eggs expelled 4 hours before had reached the middle and caudal portion of the ampulla. They stayed there until they reached an average ovulation age of 12 hours. Since the spermatozoa need a minimum time of 4 hours to travel up to the ampulla, they would meet ova ovulated about 8 hours previously. The travelling time of the sperms to the region of fertilization follows from the fact that the first fertilized eggs after a morning mating were found in the ampulla at the earliest 4 hours post coitum. The ampullar eggs of females killed before this time are still unfertilized (Tables 3 and 5). If mating took place in the evening before follicular rupture, the first spermatozoa are already in the ampulla at the time of ovulation. Therefore it is surprising not to find all the ova fertilized in the ampulla 3 hours after ovulation. At this time and in spite of the presence of sperms only 11 out of 63 eggs were fertilized (Table 5).

A short time later the proportion of zygotes increases rapidly. This finding supports the idea that the freshly ovulated hamster egg is incapable of being fertilized. The ovum needs to age in order to attain the capacity for fertilization. Table 3 indicates clearly that 4 hours after mating and at an ovulation age of 8 hours, one of 4 eggs lying in the mid-ampullar region was fertilized, and 6 of 27 ova of the caudal third. In the course of the two following hours (6 after copulation, 10 after estimated time of ovulation) even more gametes will be fertilized, whereas the eggs that arrived earlier wander further. Thus I believe that the morning mating does not cause a shift of the fertilization site. On the other hand, eggs of an ovulation age of 12 or more hours meeting the sperm when the ova are already leaving the fertilization site, show a rapidly decreasing fertilization capacity. It becomes zero when the mating occurs 8 or more hours after ovulation (Ward, 1946).

In the pronucleus stage the hamster zygote leaves the fertilization site to appear in the transitional section. We find the first eggs there 10 hours after the hypothetical time of follicular rupture. The last of the ova reach that part of the oviduct at an ovulation age of 16 hours. In the meantime, however, the first 16hour zygotes have already entered the isthmus. Thus, practically all the eggs have left the ampulla by 16-18 hours after ovulation and are found either in the transitional section, or have already entered the isthmus. Therefore it may be concluded that 20 hours after follicular rupture the greater portion of the female gametes and zygotes had left the transitional section. The presence of spermatozoa in the ampulla and fertilization do not influence the migration tempo in the ampulla, for in the control animals the arrival of the ova within the transitional section occurs between 10 and 16 hours after ovulation. Therefore, it is justifiable to assume that the eggs move relatively rapidly, within a maximum of 6 hours, through the transitional section.

From comparison of Tables 3 and 4 one receives the impression that the eggs may remain in the transitional section longer in the mated animals than in the controls. In the mated animals 10·9 per cent, of the eggs were found in the transitional section against 5·9 per cent, in the control animals. The difference between these values lies possibly outside the margin of error. Furthermore, one must not overlook the fact that 22 to 36 hours after follicular rupture 17 (26·2 per cent.) of 65 eggs were detained in the transitional section; of these 16 were fertilized. In this same time interval in the mated animals, 134 eggs (among them 114 zygotes) had reached the isthmus. In the control series, however, there were no stragglers; all ova had reached the isthmus by 22 hours. This apparent contradiction is supported by the fact that a smaller proportion of the eggs (11·3 per cent.) travel rather more slowly through the transitional section than do the principal mass and the unfertilized eggs. There are no data to explain this. It is conceivable that these retarded eggs experience a variation similar to the retarded fertilized rat and guinea-pig egg as described by Blandau & Jordan (1941) and Blandau & Young (1939).

Since very few exact investigations exist on the fertilization site of the mammalian egg, it is difficult to compare these results with others and to classify them critically. The findings of Sobotta, however, verified by Kremer (1924), were of great value in this work. The section of the tube known as the fertilization site of Sobotta connects with the ampulla and shows many ampullar characters. Consequently one is justified in stating that fertilization in the hamster and the white mouse takes place in essentially identical sections of the ampulla.

In describing fertilization of the rat egg Tafani (1889), Sobotta & Burckhard (1910), and Huber (1915) adhere closely to the presentation given by Sobotta for the mouse. They observed the fertilization site in the rat as a widened vesicular section of the ampulla which compares to the middle third of the ampulla in the golden hamster.

According to Rein (1883), Rubaschkin (1905), and Lams (1913) a similar relationship seems to exist in the guinea-pig. Even though their data are not as exact as would be desirable for comparison, it seems that the union of the two gametes in Cavia likewise occurs in the ampulla. When Hammond (1934) spoke of the proximal end of the oviduct as the fertilization site for the rabbit egg the ampulla was meant. From the data given by R. van der Stricht (1911), and by Hill & Tribe (1924), the fertilization in the cat occurs in the proximal third of the tube and the ampulla should likewise be understood.

The temptation is great to take the results based on the investigation of three representatives of the family Muridae, and to assume when the fertilization site is said to be in the ampulla that it is always the same section of the ampulla. One should be cautious about such generalizations until new investigations have brought to light further details of this question. On the basis of present findings it cannot be said that all mammalian eggs are fertilized in the same area (Strauss, 1938,1954). In the same way neither a family-specific nor even an order-specific fertilization place can be established at the present time.

This investigation was aided by the Wisconsin Alumni Research Foundation and by grants from the American-Swiss Foundation for Scientific Exchange, Inc., and the Swiss Academy of Medical Sciences.

The author wishes to express his profound gratitude to Dr. H. W. Mossman for his invitation and aid in this study, which was mostly carried out in his laboratory. Furthermore, the author is indebted to Dr. Margaret W. Orsini for some advice, help in the experiments, and for use of certain data.

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