Paper - Transuterine (internal) migration of the ovum in sheep and other mammals

From Embryology
Embryology - 20 Aug 2019    Facebook link Pinterest link Twitter link  Expand to Translate  
Google Translate - select your language from the list shown below (this will open a new external page)

العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt    These external translations are automated and may not be accurate. (More? About Translations)

Boyd JD. Hamilton WJ. and Hammond J. Transuterine (internal) migration of the ovum in sheep and other mammals. (1944) J Anat. 78(1-2): 5-14. PMID 17104941

Online Editor  
Mark Hill.jpg
This historic 1944 paper by Boyd describes the migration of the early developing embryo within the uterine tube in sheep and other mammals. Transuterine migration is described as the passage of fertilised ova from one uterine horn into the other and has mainly been described for animals with a bicornuate type of uterus.

By the same author: Boyd JD. Development of the thyroid and parathyroid glands and the thymus. (1950) Ann R Coll Surg Engl. 7(6): 455-71. PMID 14790564

Modern Notes:
Sheep Development

Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Transuterine (internal) Migration of the Ovum in Sheep and other Mammals

Boyd JD. Hamilton WJ. and Hammond J.

Anatomy Department, London Hospital Medical

Anatomy Department, St Bartholomew’s Hospital Medical College.

School of Agriculture, Cambridge University.


In the course of investigations on the genital tract of pregnant sheep, ova, blastocysts and embryos of known age were found in positions that appear to throw some light on the problem of the transuterine (‘internal’) migration of the ‘ovum’.§ In examining the literature it was found that while the subject of migration of the ovum has been dealt with by a number of investigators, particularly Corner (1921), no complete review was available. In addition, many investigators have implied, in their data, the occurrence of migration without having stated explicitly that it had taken place.

The term internal migration is generally used to describe the passage of the ovum (or its derivatives, the blastocyst or chorionic sac) from one uterine horn to the other by way of a common uterine body in those species with a bicornuate uterus. External migration is the term used to describe the phenomenon of the passage of an ovum shed from one ovary across the peritoneal cavity to the ostium of the opposite uterine tube and thence to the opposite uterine horn. Frankel (1924) suggested that the term uterine migration should be used for the phenomenon of internal migration and peritoneal migration for external. We, however, prefer the terms transuterine and transperitoneal for the two types of migration.

  • Theoretically, the term ovum should not be used after the commencement of cleavage. By long-established practice, however, the term is loosely applied to the early developing embryo.

We wish to thank Dr John Hammond, F.R.S., for additional data which make our conclusions on the frequency and distribution of corpora lutea and embryos in the sheep more significant.

An account is given of our own observations in the sheep, and this is followed by a review which shows that transiiterine migration is of widespread occurrence in Eutheria.

Transuterine Migration In Sheep

Most of the sheep were of mixed or undetermined breed; the uteri were collected and examined in most cases within 15 min. of the death of the animal thanks to the co-operation of the slaughterhouse authorities. In a number of cases (Table 1) the side on which ovulation occurred is known; in many cases, however, it was known that two ovulations had occurred from one ovary but the side was not recorded. A correlation between ovary and uterine horn was, oflcourse, available.

Table 1 and Text-fig. 1 summarize the distribution of corpora lutea and the number and situation of pregnancies in the seventeen cases of multiple ovulation in the series which we have examined specifically for evidence of migration. It will, be seen that in five of the sheep two cgrpora lutea were found in one ovary: while the resulting conceptuses were found one in each uterine horn (Text-‘fig. 1 C). These included one pair of twins of about 20 days (late somite stages, 3-5 mm. long) and four pairs of twin embryos varying between 12 and 40 mm. C.R. length.

In four sheep of this series there were two ovulations in a single ovary with both the resulting conceptuses in the corresponding horn. These included one pair of embryos in which there was a normal embryo of 26 mm. C.R. and a 6 mm, degenerated abortus. The other three cases were 10-, 12- and 13-day blastocyst twins (Text-fig. 1 B). x .

In two sheep two recently ruptured follicles were found in one ovary, and in each of these cases two unfertilized ova were washed out of the corresponding tube (Text-fig. 1 A).

In two sheep two corpora were found in the left ovary, but in each case a single conceptus was found in the right uterine horn. In each case the embryo wasabout the 30 mm. stage (Text-fig. 1 E).

In one sheep two corpora were found in the right ovary and two 19-day embryos were found in the right horn, but their chorionic sacs extended through the unpaired ‘body’ into the other uterine horn (Text-fig. 1 D). In one sheep there were two corpora in the right ovary, but only one embryo, of about 20 days’ gestation, was found in the right horn though its chorionicsacextended, as in the previous case, into the left horn. Finally, in two sheep two corpora were found in the right ovary and there was one ‘embryo in the right horn and one in the unpaired body of the uterus (Text-fig. 1 F). These were both comparatively gzte pregnancies, the embryos measuring about 16 cm. C.R. length. The left horn in each case was much smaller than the right and the uterine body was larger than normally found in twin pregnancies.- In each of these sheep the chorions of the embryos had fused to form a single sac and, in one, the amnions were in contact and firmly united but the amniotic cavities were separate. .

In the series just described, in which there was multiple ovulation in one ovary, the conditions found can be summarized,as follows: (1) ova in the corresponding tube; (2) two blastocysts in the corresponding uterine horn; (3) older embryos situated one in each horn; and (4) intermediate stages, as demonstrated in Text-fig. 1 F.

It seems noteworthy that in the one case where two embryos at a relatively advanced stage were found in a single horn one was atrophic.

In all the other more advanced twin pregnancies the embryos were either one in each horn or one in one horn and the other in the common uterine body.

suggest that migration (transperitoneal or trans-uterine) is unusual in single pregnancies in the sheep.

In fifteen sheep with two corpora lutea in one ovary one embryo was found in each uterine horn and consequently migration must have occurred. In twelve sheep there was a single corpus luteum in each ovary with a pregnancy in each horn. In one sheep only were there two corpora lutea in one ovary and two embryos in the horn of the same side. In no case with a single corpus luteum in each ovary were there two embryos found in one horn. One case of triple ovulation showed three corpora lutea in a single ovary and only one pregnancy in each horn, the third ovum presumably not having been fertilized or the resulting embryo having degenerated. Another case of triple ovulation had two corpora lutea in one ovary and one in the other and a corresponding arrangement of the embryos in the uterine horns. In one case in which four corpora lutea were found, one in the right ovary and three in the left, only one embryo was found in each horn.

Table 1. Data for transutefine migration in double ovulations ,

State of development

25 mm. embryos

40 mm. embryos

12 mm. embryos

14 mm. embryos

20 day embryos

12 day blastocysts

One 26 mm. embryo and one 6 mm. abortus‘ 13 day chorionic sacs

10 day blastocysts

2 unsegmented ova in tube corresponding with ovary in which ovulations had

2 unsegmented ova in tube corresponding with ovary in which ovulations had

30 mm. embryo 30 mm. embryo 19 day embryos 20 day embryo

160 mm. embryos*

Sheep no. Ovulations Pregnancies W. 1 2 in right ovary l in each horn W. 4 2 in right ovary l in each horn N. 12 2 in one ovary 1 in each horn N. 16 2 in one ovary .1 in each horn N. 26 2 in one ovary 1 in each horn Sp. 9 2 in left ovary 2 in left horn N. 31 2 in one ovary 2 in horn of same side Sp. 4 in one ovary 2 in horn of same side Sp. 8 2 in one ovary 2 in horn of same side N. 17 one ovary , occurred N. 32 2 in one ovary occurred W. 2 ~ 2 in left ovary 1 in right horn W. 3 2 in left ovary 1 in right horn Sp. 15 2 in right ovary ~ 2 in right horn (chorionic sacs extended into left horn) W. 5 2 in right ovary 1 in right horn (chorionic sac extended into left horn)

W. 6 2 in right ovary 1 in right horn

1 in fused horn region W. 7 2 in right ovary 1 in right horn

1 in fused horn region

160 mm. embryosf

The umbilical cords of both embryos were attached to the medial side of the right horn, the lower close to the junction with fused horn. The right horn was much larger; the left horn gradually tapered from the fused horn region. The amnions were fused.

1' Both embryos were attached to the medial side of the right horn. The amnions were not fused but the chorions were.

Whether one of the two‘embryos in Text-fig. 1 B would have migrated at a later stage to the body or opposite horn, or have undergone atrophy, must remain a matter for speculation.

In addition to the above series in which the-age or size of the conceptuses are known within narrow limits data are also available, through the courtesy of Dr J. Hammond, F.R.S., on a much larger series of multiple pregnancies which show that migration of embryos from one horn to the other must have occurred. In this series of ‘seventyeight pregnant sheep there were forty-six with a single corpus luteum in one ovary and a pregnancy in the corresponding horn. There was only one sheep with a single corpus luteum in .one ovary and a pregnancy in the opposite horn. This appears to

The fifteen cases in which there were two ovulations from a single ovary, and a distribution of the embryos one to each h_orn, provide further convincing evidence of the reality and frequency of migration in the sheep, for in only one case were two corpora lutea in a single ovary associated with two embryos in a corresponding horn. Further, the fact that migration was not observed in embryos with a single ovulation from each ovary suggests that the distribution is not random but appears to correspond to the spacing of eggs in polyovular mammalian species.

Boyd1944 text-fig01.jpg

Text-fig. 1. Schematic representations of the relatignships between two ovulations from a. single ovary and the distribution of the resulting conceptuses as found in our series of sheep. (For details see text.)

Although transperitoneal migration is possible in the sheep, since the ovaries are not in a closed ovarian bursa, the data in Table 1 are strongly in favour of transuterine migration. Further, in all those sheep in which there was a single‘ ovulation the conceptus, with one -exception, was found in the same tube or uterine horn as that of the ovary from which ovulation occurred.

Structure of the Uterus in the Sheep

The uterus in the sheep is a typical ungulate bicomuate uterus with two horns, a short common body and a cervix. To the/naked eye the appearance of the mucosa of the body is very similar to that of the horns, possessing typical caruncles (cotyledons) with melanin-like pigmentation.

Detailed histological studies have been made on the genital tract of the sheep at different stages in the oestrous cycle by Casida &. McKenzie (1932), Cole & Miller (1935) and McKenzie & Terrill (1937). None of these investigators, however, have specifically stated that the endometrium of the body is identical in structure with that of the comua. As the chorion comes into intimate and, presumably, functional contact with the mucosa of the corpus uteri We have examined its microscopic structure and compared it with that’ of the cornua. The appearances are essentially similar both in intercaruncular (cf. Pl. 1, figs. 1 , 2) and caruncular regions. A typical caruncle of the body is shown in P1. 1, fig. 3. The lining of the cervix is very different; glands are almost completely absent and the mucosa is raised up into complicated viHous folds (Pl. 1, fig. 4).

In view of the possibility that cilia may be involved in the intra-uterine transference of ova we examined the endometrium with this point in mind. No cilia were apparent.


Migration of ova in eutherian mammals

Bischoff (184-2) drew attention to the fact that the number of corpora lutea usually corresponds with the number of embryos, but in the rabbit he occasionally found, especially in the later stages, fewer embryos than corpora lutea. This he explained by the abortion of some of the embryos. This has been confirmed by many investigators since (see Hammond, 1921, 1941, for literature). Bischofif pointed out that in the rabbit as a rule just as many ‘eggs’ are found in each tube or horn of the uterus as there are corpora lutea in the corresponding ovary. In dogs, however, he made the important observation that ova are occasionally distributed in the uterine horns in such a fashion as to be explained only by ‘Ueberwanderung des Eies’ (migration) from one uterine horn to the other as the number of corpora lutea in each ovary did not correspond with the number of the embryos in the horn. In his paper on the early development of the dog (1845) Bischoff gave more details on this ‘wandering’ and commented on the possible method by which eggs .could be moved from one uterine horn to the other. He concluded that it was most likely due to uterine contractions. He also considered the possibility that the number of corpora lutea in the ovary may be no certain criterion of the number of eggs that have been shed, since there may have been pluriovular follicles and some ‘eggs may have been aborted. He concluded, however, that such an explanation is extremely unlikely in view of the need for the coincidence required to make the number of aborted ova on one side exactly balance the excess on the_other; he considered it much more likely that migration occurred under the same (unknown) control that arranges the spacing of the eggs in one horn of the uterus in the dog or other polyovular animals in such a way that they have proper room for development. His conclusion on ‘Ueberwanderung des Eies’ in the dog is that it is ‘eine sehr bemerkenswerthe, aber sicher ausgemachte Thatsache’. In later papers on the development of the guinea-pig (1853) and the European roe-deer (1854), Bischoff also described migration of ova. Leuckart (in Bergmann & Leuckart, 1857) confirmed Bischoff’s findings in the guinea-pig, but Reichert (1861) contradicted this and doubted very much if the phenomenon occurred in any mammal. Bischoff (1842, 1859—in a letter to Kussmaul, p. 318) himself never found migration in the rabbit, which he attributed to the fact that here there are completely separated uteri opening separately into the vagina.

Since Bischoff’s time several investigators have made specific contributions to the subject of migration of the ovum, and a number of others have referred incidentally to it or have presented data from the examination of which its occurrence or not may be deduced. The contributions of these workers are summarized in Table 2.

Migration of the egg can either be from the ovary to the opposite uterine tube in those animals in which there is no completely closed bursa ovarica (so-called external or transperitoneal. migration) or

it may be from one horn of a bicornuate uterus to the other by way of a longer or shorter common uterine ‘body’ (internal or transuterine migration). External migration is theoretically possible in all mammals without an ovarian bursa or with the latter in communication with the peritoneal cavity. A number of cases have been recorded for man (see Kussmaul, 1859; Sippel, 1901; and Grosser, 1927); Sippel, indeed, has emphasized the frequency of the contra-lateral situation of the corpus luteum in

Tranlsuterine migration of the ovum

Table 2. Trtmsutcrine (‘internal’) migration in mammals








‘ Deer (Capreolus capreolus)

Procawiu. capensis



Cat Ferret Badger



Vespertilio murirlus Veaperugo pipistrellus

Rhinolophuaferrum equinum

M olos8u.s crassicauclalus Vesperugo rnurirma

Observer (names of ob servers who specifically

describe migration are italicized)


. Hausmann

Kelly _ K up fer Warwick

Bonnet Cursor» Carson

Hausmann Present data

Quinlan Tsukaguchi

Bergmann Day Kaltner

K upfer

Day K edrov


Turner Wisloclci

' Bischoff Bonnet Hausmann Sparapani Splegelberg

Hill dc Tribe Hammorad db Marshall Fischer

Personal observation



Duval Hamlett V Van der Slrioht


50% of cases ‘.7 1 case in 17

7 cases in 29 199 cases in 469

3 cases in 118 2 cases in 5

2 cases in 36 I casein 16

1 case (triple pregnancy) 1 case, at least, in 14

1 case in 50

1 case in 1000 0 cases in 300 1 case in 1000

5 cases in 7

4 cases in 12

Observed several times 1 casein 12 2 (? 3) cases in 17

1 case in several hundred

1 case


1 case


Remarks '

See footnote 1


Also experimentally

Double pregnancies Single pregnancies

Quoted by Curson - «

See ‘footnote 2 Personal communication

See footnote 2

See—t"ootnote 3

Segiootnote 4 Quoted by Kussmaul (p. 319)


Internal migration considered possible

The blastocysts of these bats always imbed in the right horn although there is ovulation from either ovary. Hence migration must occur

(In Glossophaga soricina (Hamlett), where the uterus is simplex, and in Cynopterus rnargimrtus (Keibel), where the uterine horns open separately into the vagina, migration has not been observed) internal migration a much more likely explanation.


(1) In 1915 Corner considered external migration more probable; in 1921 he produced evidence making

(2) In the cow no records have been made of the migration in twins. ll?-ergmann in two cases and Kupfer in seventeen, in none of which both ovulations were in the same ovary, failed to find migration. Lillie (1917 and 1923) gives no data on corpora lutea in his extensive study of free-martin twins in cattle.

(3) Kedrov, by rectal examination of 574 mares during 804 oestrous cycles, found, that ovulation occurs 15—20% more often in the left ovary. As pregnancies were observed more frequently (25-30 %) in the right uterine horn he concluded that intrauterine migration must occur. '

(4) Quoted by Schmaltz (p. 233) as having found external (peritoneal) migration by experiments comparable to those of Leopold on the rabbit.

Table 2

Observer (names of observers who specifically describe migration are Type italicized) Insncrrvona ‘ Sorex amneus Linn. P Brambell Soreav minulus Linn. Brambell Talpa Personal observations Erinaceus Deanesly Pnrmaras Lemur mfipes Turner RODENTIA Rabbit Leopold Asdell Baur Guinea-pig Bischoff Leuclcart Albino rat Hanson & Boone Slanalcer Field vole Brambell

tubal pregnancy and explains the occurrence of the condition by the fact that the time necessary for transperitoneal migration results in the egg reaching the opposite tube at a time when it is ready for implantation. Williams (1941) also has shown that in a considerable number of cases of tubal pregnancy the corpus luteum was not in the ovary corresponding with the pregnancy in the tube but in the opposite one, which indicates that transperitoneal migration must have occurred. Leopold (1880) and Baur (1921) claim to have demonstrated external migration in the rabbit, and Corner (1915) originally held that this was of frequent occurrence in the pig (but see later). Our sheep material, as has already been stated, throws no light on this question.

Internal migration has been described, among carnivores, in the dog by Bischoff (1842, 1845), in the cat by Hill & Tribe (1924) and in the ferret (experimentally) by Hammond & Marshall (1930). ‘We have found evidence for migration in a vixen in which there were three corpora lutea in the left ovary and one in the right; the foetuses (65 mm. C.R. length) were distributed two to each horn of the uterus.

In those carnivores (the European badger and possibly the American badger, certain martens and bears) which show the phenomenon of delayed implantation (‘ Entwicklungspause ’) one would expect to find transuterine migration, from one uterine horn to the other, more frequently than in the cat, dog and ferret, for in such cases there is more time available for ‘spacing’ of the eggs. Unfortunately, the data recorded in the literature on delayed implantation in carnivores does not enable us to determine if such migration occurs. Fischer (1931), however, in his work on delayed implantation in Meles meles, expresses the opinion that transuterine migration does occur in this carnivore.

_ 13 cases in ‘? 47


Frequency Remarks

28 cases in ? 99

N 01; possible to correlate corpora lutea with pregnancies

Not possible to correlate corpora

lutea but embryos are fairly

evenly distributed between the , ‘two home

1 case in 4

External migration only } and, experimentally; by'ParIces

Migration denied by Reicherl, Squier, K inmzy, Nicol and K elly

N o evidence for migration N o evidence for migration

No evidence for migration

Among the Cheiroptera there are at least five species with bicornuate uteri in which there is abundant ‘evidence for uterine migration of ova and blastocysts (see Table 2). These species are of particular interest in that implantation is almost invariably in the right horn although ovulation may occur in either ovary. In Glossophaga soricina (Hamlett, 1934), with a uterus simplex, and in Cynopterus marginatus (Keibel, 1922), where the uterine _horns open separately into the vagina, migration, on the data presented, does not appear to occur.

In the Insectivora, Brambell (1935, 1937) has shown conclusively that transuterine migration occurs in Sorea: araneus and in S. minutus. In Erinaceus europaeus, Deanesly (1934) did not find it possible to count the corpora lutea, and hence correlation of them with the number and distribution of the embryos could not be achieved. She draws attention, however, to the fact that the embryos are distributed fairly evenly between the two horns. In our own small series of pregnant specimens of

Migration denied by Bischofi Talpa europea we were also unable to count the corpora lutea with any feeling of certainty, and hence are unable to state if migration occurs in this insectivorei‘ .

In lower primates with bicornuate uteri few workers have given data on the distribution of the corpora lutea and the situation of the pregnancies. It is interesting to note, however, that Turner (1876) gave details of four pregnancies in Lemur rufipes -which enable one to state that migration (transuterine or transperitoneal) must have occurred in one of them.

A few cases in the clinical literature suggest that transuterine migration may occur in the human in cases of interstitial ectopic pregnancy. The literature on this subject has been reviewed by Schlink (1924) who describes several well-authenticated cases. It is a theoretical possibility in cases of pregnancy in bicomuate uteri.

The data presented in this paper, for the sheep, and the literature on the development of the sheep, goat, cow, horse, pig, deer and Procavia, show quite conclusively that migration occurs frequently in the ungulates. This conclusion is supported by the experimental _work of Warwick (1926) and Kelly (1928) who demonstrated transuterine migration in the sow when one uterine tube and the corresponding ovary had been removed. The frequency of migration is variable from species to species, being, apparently, most common in the pig and horse, less common in the sheep and goat, and rare in the cow. It is diflicult to explain this variability, as the anatomical conditions are very similar in all of these species. It, presumably, can be attributed to species differences in the forces, whatever they may be, which cause the distribution of the eggs. Multiple pregnancy might be a contributory factor in the frequency of migration in the pig, but that it is not the only factor is shown by the apparently much greater frequency of migration in the horse as compared with the cow, although these two species are mainly monovular. Our ‘results in the sheep, and those briefly recorded by Curson (1934), show that migration is common, in this ungulate, in double pregnancies resulting from two ovulations in a single ovary, but is rare in single pregnancies. It was found only once in all the sheep (95) on which we have data. Curson found it twice in thirty-six sheep.’

Among the rodents, transperitoneal migration has been described by Leopold (1880) and by Baur (1921) in rabbits in which one ovary had been removed and the opposite uterine tube cut and tied. Baur found migration in five_out of twelve experimental animals, and in one animal found as many as ten embryos in the uterine horn of the side on which the ovary had been removed. Asdell (1924) and Hammond (1935) also record that such migration occurs in the rabbit. Bischoff (1842) by comparison of corpora lutea and distribution of embryos in the rabbit found no evidence of migration. Parkes (1924), too, who, like Leopold and Baur, investigated the problem experimentally, found that not a single conception occurred in six rabbits in which one uterine tube and the contralateral ovary had been removed. Parkes suggested that Leopold’s results might have been due to regeneration of the ovary on the side on which ovariectomy had been performed, but he admits that external migration may occasionally occur. _Parkes does not refer to the work of Baur which not only verified-Leopold’s results but appears to have been carefully carried out and to have avoided the possibility of even the recanalization of the sectioned tube or of regeneration or incomplete removal of the ovary on the side in which pregnancy ensued. Further, Baur’s counts of corpora lutea in the single remaining ovary agree completely with the number of pregnancies in the opposite uterine horn, and an acceptance of his results seems to indicate that not only can external migration occur in the rabbit, but that, under the conditions obtaining in his experiments, it is extremely common. In the rodents which possess a completely closed ovarian bursa (e.g. mouse, rat and field vole) transperitoneal migration is obviously impossible, and has been demonstrated to be so by Hanson & Boone (l924—5) and by Slonaker (1927) in the albino rat.

Transuterine migration is extremely unlikely in those rodents which possess uterine horns (better called right and left uteri) which open separately into the vagina. Leopold (1880) believed that his experiments on the rabbit demonstrated that both internal and external migration occurred. His results, however, were not checked by post-mortem examinations, and Baur’s later experiments (1922) seem to demonstrate quite clearly that transuterine migration does not occur in the rabbit. Transuterine migration has been described by Bischoff (1853) and Bergmann & Leuckart (1857), on the basis of corpora lutea counts, in the guinea-pig, and in this species it is theoretically possible as there is a short common uterine segment. Kelly (1928), however, has shown that the uterine partition in the guinea-pig nearly reaches to the vagina and the experimental investigations of Kinney (1924), who performed unilateral ovariectomy in nineteen guinea-pigs and found no case of migration in subsequent pregnancies, appear to demonstrate that in spite of the presence of a short common segment, migration does not, in fact, occur in this species. This conclusion is supported by the descriptions of Reichert (1861), Squier (1932) and Nicol (1934). Transuterine migration, then, of the type found in Ungulata, Carnivora, Cheiroptera, ’

‘Insectivora and at least one primate has not yet been demonstrated conclusively to occur in any of the rodents which have been studied with specific reference to such migration.

Probable mechanism

The question of the entry of the ovum into, and its migration through, the uterine tube has been discussed and the literature summarized by Westman (1926) and Grosser (1927); our material contributes no evidence on this problem. ' Our investigations involve the consideration of the mechanism of migration after the entry of the ovum into the uterus. In many mammals this involves the passage of the ovum or ova and their spacing, in multiovular species, either in one or both horns.

The problem is rather different in those species where the blastocyst remains relatively small and becomes early attached to, or actually penetrates. the endometrium, from those in which the chorionic sac becomes enormously enlarged and only a placenta of the epithelio-chorial or syndesmo-chorial type is developed. Even in species (e.g. rabbit) with a uterus duplex, in which transuterine migration is improbable, the problem of how the embryos become regularly scattered (spaced) and orientated in the uterus is unknown (see Mossman, 1937).

In most species at the time of the entry of the segmenting egg or morula no one part of the horn appears to be more favourable for attachment, nevertheless the embryos in most species become more or less regularly spaced; how this is achieved

is unknown, but it ‘obviously involves two main factors: (1) a mechanism for the transport of. the ova, and (2) a mechanism which prevents the implantation ‘of one ovum in close proximity _to another.

Mossman (1937) suggests that the uterine mucosa in the immediate neighbourhood of an implanted ovum becmnes refractory to the attachment of any other ovum. The migration of ova, blastocysts or chorionic sacs in those species (with bicornuate uteri) in which it can occur is obviously only a special instance of the general problem of the spacing of the embryos. The attempt at spacing, however, may not be completely successful; one embryo may remain in the common body of the bicornuate uterus,.as was found in sheep nos. W 6 and W 7, and as has been recdrded by Brambell (1935) in Screw anmeus and again (1937) in S. minutus. In Cheiroptera the migration is associated with a specialized receptive area in the right uterine horn.

There is no precise knowledge of the nature of the process involved in the migration of ova, blastocysts or chorionic sacs. It was, however, early recognized -that ova and blastocysts have no inherent motility but that chorionic sacs may show slight ‘ creeping’ growth. The forces must, therefore, be extrinsic to the ovum, and here there appear to be only two possibilities: activity of the uterine muscle or action of the ciliated endometrial epithelium. It would seem that the ‘latter is unimportant, since cilia are not conspicuous features of the endometrial epithelia of most types. Lim & Chao (1927) have shown that the reversal of the middle portion of a'uterine horn in the rabbit not only permits of pregnancy but also does not inter‘fere with the distribution of the ova, showing that ciliary activity playsno essential role in the transport of ova within the uterus which must, therefore, depend wholly on uterine muscular contractions. That the contractions of the uterine muscle must play the most significant role was suggested by.

Bischoff (1842) in his original account of internal migration. Volker (1922), in his Normentafeln on the development of the Spermophilus, describes the peristaltic uterine waves as ‘seizing’ the ova and carrying them onwards on the mesometrial border of the uterine lumen. In the interval between the peristaltic waves Volker believes that the ova can settle by gravity into the folds of the antimesometrial border of the uterine lumen, where they become implanted.

It is well established that uterine activity at first increases and then gradually diminishes following ovulation. Keye (1923) has described two types of spontaneous contractions in the isolated uterus of the sow; a major type upon which can be superimposed minor contractions. At the time of ovulation and during the passage of the ova along the uterine tubes the major contractions alone are present; the minor contractions begin with the functional development of the corpus luteum and increase until about the 13th day following ovulation. Keye believes that the minor contractions are concerned with the transport of ova through the uterine canal and their arrangement in a regular order for implantation. The full, establishment of pregnancy alters the activity of the uterine musculature and causes a marked diminution of both types of contraction waves. Keye suggested that his physiological findings could be correlated with Co'rner’s (1915) histological picture of the corpus luteum.

Lim & Chao (1927) confirmed the presence of peristaltic movements and also showed that antiperistaltic movements occurred. Their investigations were carried out on the- rabbit in which transuterine migration does not occur, but their results can obviously be applied to explain the passage of blastocysts or even chorionic sacs (in those animals with non-deciduate placentae) into the opposite uterine horn from that which the segmented ovum or morula first entered. While these results of Keye and Lim & Chao seem to demonstrate a possible mechanism for the transuterine migration of the ovum the recent summary on the physiology of the uterus by Reynolds (1939) appears to show that the myometrium is quiescent long before ova reach the uterine lumen in mammals.

It is obvious that whatever forces are involved in transuterine migration they cannot be unidirectional, for the ova ‘ascend’ into the opposite horn. This interpretation is supported by Lim & Chao’s experiments on reversal of uterine segments in the rabbit. Reynolds suggests that ‘perhaps the weak unco-ordinated motility which the uterus exhibits at this time is concerned in some way, but as yet no evidence is available to show whether or not this is so’. Reynolds concludes that, ‘While it is clear that the mechanisms concerned in spacing’ (and, we would add, in transuterine migration) ‘are considerable, their nature is totally unknown at the present time’. We would, however, substitute insufiiciently for totally in this statement, as the available physiological evidence clearly suggests that rhythmic peristaltic and antiperistaltic contractions of the uterine muscle may be among the main factors involved.

Significance of intra-uterine migration

Bischoff suggested that intra-uterine migration was a mechanism for balancing the number of embryos in each uterine horn when there has been a gross disparity in the number of ovulations from each ovary. Corner has supported this interpretation and advances the hypothesis that the phenomenon of transuterine (internal) migration has a practical utility in the pig in that it assures that the individual embryos of large litters should each find a fair share of space in the uterine cavity. This quasi-teleological explanation does not hold for species which are normally monovular. Thus transuterine migration is extremely rare in cows but common in mares. It has never been recorded for twins in cows but is, as we have shown, common in twins of sheep. These differences may be explained in part by subtle differences in the activity of the uterine musculature in the ungulates and in part On the fact that with only one or two pregnancies the need for spacing is not so urgent, especially as the chorionic sacs can later extend around into the vacant horn. Polyovulation is obviously'a factor in the sheep where migration is frequent with double ovulations (from one Ovary) but rare with single ovulations. On the other hand, in the horse, with single ovulations as the rule, intra-uterine migration is common. This is also true of many Cheiroptera. Polyovulation, then, is not the sole factor in the production of intra-uterine migration.


  1. Data are recorded which indicate that transuterine migration is of frequent occurrence in the sheep when double pregnancy results from two ovulations in a single ovary.
  2. The histological appearances of the uterine cornua and body in the sheep are described.
  3. The literature on transuterine Jmigration is summarized and discussed.

The cost of the material utilized in this investigation was partially defrayed by a grant to _two Of us (J. D. B. and W. J. H.) from the Research Fund of the University of London. We wish to express our thanks to Mr E. Park for technical assistance.


ASDELL, S. A. (1924). Brit. J. Exp. Biol. 1, 473.

BAUR, H. (1921). Mitnch. med. Wschr. 68, 1103.

BAUR, H. (1922). M itnch. med. Wschr. 69, 48.

BERGMANN, C. & LEUCKART, C. G. F. R. (1857). Vergl. Anat. u. Physiol. u.s.w. Stuttgart. BERGMANN, R. (1922). Arch. Tierheillc. 47, 292.

Brscnorr, T. L. W. (1842). Entwicklnngsgeschichte des Kaninchen-Eies. Braunschweig.

Brscnorr, T. L. W. (1845). Entwiclclungsgeschichte des Hunde-Eies. Braunschweig.

BISCHOFF, T. L. W. (1853). Entwiclclungsgeschichte der M eerschweirwhen. Giessen.

Brscnorr, T. L. W. (1854). Entwicklangsgeschichte des Rehes. Giessen. ,

BONNET, R. (1884). Arch‘. Anat. Entw. Amzt. Abt. 170.

BONNET, R. (1897). Anat. Hefte, 9, 419.

BRAMBELL, F. W. R. (1935). Philos. Trans. B, 225, 1.

BRAMBELL, F. W. R. (1937). Proc. Zool. Soc. Lond. p. 957.

BRAMBELL, F. W. R. (1939). Proc. Zool. Soc. Land. A, 109, 133.

CASIDA, L. E. & MCKENZIE, F. F. (1932). Res. Bull. Mo. Agric. Exp. Sta. no. 170.

COLE, H. H. & MILLER, R. F. (1935). Amer. J. Anal.‘ 57, 39.

CORNER, G. W. (1915). Oontr. Embryol. Carney. Instn, 5, 69.

CORNER, G. W. (1921). Johns Hopk. Hosp. Bull. 32, 78. CURSON, H. H. (1934). Ortderstepoort J. Vet. Sci. 3, 133.

DAY, F. T-. (1940). J. Agric. Sci. 30, 244. ‘ DAY, F. T. (1943). Personal communication.

DEANESLY, R. (1934). Philos. Trans. B, 223, 239.

DUVAL, M. (1895). J. Anal. Physiol. 31, 93-160. FISCHER, E. (1931). Anat. Anz. 72, 22.

FRANKEL, L. (1924). Physiologic interne weiblichen Genitalorgane. Halban-Seitz, 1. .

GROSSER, O. (1927). Frahentwiclcldng Eihautbildung and ' Placentation des M enschen and der Sciugetiere. Bergmann.

HAMLETT, G. W. D. (1934). Anat. Anz. 79, 146.

HAMMOND, J. (1921). J. Agric. Sci. 11, 337. HAMMOND, J. (1935): Trad. Dinam. Razvit. 10, 93. HAMMOND, J. (1941). Biol. Rev. 16, 165. '

HAMMOND, J. & MARSHALL, F. H. A. (1930). Proc. Roy. Soc B, 105, 607.

HANSON, F. B. & BOONE, 0. (1924—5). Anat. Rec. 29, 384.

HAUSMANN, U. F. (1840). Ueber die Zeugung and Entetehung des wahren weiblichen Eies bei der Siiugetiere [and Menschen. Hannover.

HILL, J. P. & TRIBE, M. (1924). Quart. J. Micr. Sci. 88, 513.

KALTNER, A. (1923). Zbl. Gyruilc. 4-7, 1449. K-EDROV’, V. K. (1939): Dokl. seljelcahaz. Nank. 2/8, 65.

KEIBEL, F. (1922). Arch. milcr. Anal. 96, 528.

KELLY, C. L. (1928). Anat. Rec; 40, 365.

KEYE, J. D. (1923). Johns Hoplc. Hosp. Bull. 34-, 60.

KINNEY, P. B. (1924). Amer. J. Obstet. Gynaec. 8, 198;

KUPFER, M. (1920). Denlcschr. Schweiz. Natnrf. Gas. 56. V

KUPFER, M. (1920). Vjschr. natnrf. Ges. Zurich, 65, 375.

KUSSMAUL, A. (1859): Von dem M angel der Verlcilmmerung nnd Verdopplung der Gebdrmutter, van der N achempfdngniss und der Uberwanderung des Eies. Wurzburg.

LEOPOLD, G. (1880). Arch. 16, 22.

LILLIE, F. R. (1917). J. Exp. Zool. 23, 371.

LILLIE, F. R. (1923). Biol. Bull. (Woods Hole, 54-, 47.

LIM, R. K. S. & CHAD, C. (1927). Chinese J. Physiol. 1, 175.

MCKENZIE, F. F. & TERRILL, C. E. (1937). Res. Bull. Mo. Agric. Exp. Sta. no. 264.

Mossmnx, H. W. (1937). Czmtr. Embryol. Carney. Instn, 26, 129. .

NICOL, T. (1934). Proc. Roy. Soc. Edinb. 54-, 56.

PARKES, A. S. (1924—5). J. Physiol. 59, 357.

REICHERT, C. B. (1861). Abh. preuss. Aloud. Wt'ss._9'l.

REYNOLDS, S. R. M. (1939). Physiology of Uterus. London:Hamilton.

SCHLINK, H. H. (1924). Med. J. Aust. 23, 555.

SCHMALTZ, R. (1921). Das Geschlechtsleben. der Haussiiugetiere. Berlin.

SIPPEL, A. (1901). Zbl. Gynaek. 25, 289.

SLONAKER, J .' R. (1927). Amer. J. Physiol. 81, 620.

SQUIER, R. R. (1932). Contr. Embryol. Carneg. Instn, 23, 223.

TSUKAGUCHI, R. (1912). Anat. Hefte, 4-6, 415.

TURNER, W. (1875). Proc. Roy. Soc. 24-, 151.

TURNER, W. (1876). Philos. Trans. 166, 569.

VAN DER STRICHT, O. (1911). 0.R. Ass. Anat. 13, 1.

VOLKEB, 0. (1922). Ncrrmentaf. Wirbel. 13. '

Winwmx, B. L. (1926). Anat..Rec. 33, 29.

WESTMAN, A. (1926). Acta gynec. sound. 5, Suppl. 1.

WILLIAMS, J. W. (1941). Obstetrics. New York: Appleton:

WISLOCKI, G. B. & VAN DER WESTHUYSEN, 0. P. (1940). , Oontr. ljjmbryol. Carneg. Inst, 28, 65.

Explanation of Plate

Fig. 1. Section through the glandular region of the endometrium of the uterine cornu. x 150.

Fig. 2. Section through the glandular region of the endometrium of the uterine body. x 150.

Fig. 3. Section through 9. caruncle (cotyledon) of the uterine body. A section through a cal-uncle of the horn has an identical appearance. The characteristic melanimlike pigment is seen immediately beneath the epithelium. x 150.

Fig. 4. Section (of the cervical mucosa. x 150.

Cite this page: Hill, M.A. (2019, August 20) Embryology Paper - Transuterine (internal) migration of the ovum in sheep and other mammals. Retrieved from

What Links Here?
© Dr Mark Hill 2019, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G[Category:1940's]][