The Eggs of Mammals (1936) 8

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Pincus G. The Eggs of Mammals. (1936) The Macmillan Company, New York.

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The Eggs of Mammals

The Eggs of Mammals (1936): Introduction | The Origin of the Definitive Ova | The Growth of the Ovum | The Development and Atresia of Full-Grown Ova and the Problem of Ovarian Parthenogenesis | Methods Employed in the Experimental Manipulation of Mammalian Ova | The Tubal History of Unfertilized Eggs | Fertilization and Cleavage | The Activation of Unfertilized Eggs | The Growth and Implantation of the Blastodermic Vesicle | Summary and Recapitulation | Bibliography | Figures | Historic Disclaimer

Chapter VIII The Activation of Unfertilized Eggs

We have seen that the fundamental control of the cleavage mitoses is alike in rabbit and sea-urchin ova. We shall now inquire whether the activation of mammalian eggs is also similar to that of other forms.


With the exception of the three 2-cell rat eggs described by Mann (1924) there are no observations of a possible normal parthenogenetic development of unfertilized tubal eggs in vivo. With the exception of a single observation by Champy (1927), the first investigation of the behavior of unfertilized tubal ova placed in tissue culture is that of Pincus (1930). His data are presented in Table XVII.


TABLE XVII

The Development OF Unfertilized Rabbit Ova in Culture. (From Pincus, 1930)

Age of Ova

(Hours AFTER Cop

Number

Medium

Examined (Hours in Cul

Description

Number Divided

Number Undi


ulation)



ture)


(1)



1

RPRE

44

1 — unsegmented



1

(2)



4

RPCE

48

3 — unsegmented 1 — in 3 regular cells

1

3

(3)



4

RPCE

48

4— unsegmented



4

(4)

11 9

1

CPCE

48

1 — several polar bodies (?)

1 CO

(?)

(5)

11 25

5

RPRE

24

3 — unsegmented 1 — 8 regular cells 1 — 4 regular cells

2

3

(6)

11 40

2

RPRE

48

2 — unsegmented



2

(7)

12 5

5

RPRE

47

3 — unsegmented 2— in 12 to 16 regular cells

2

3

(8)

12 30

6

RCPCE

27

1 — in 2 regular cells 1 — in 3 regular cells 1 — in 4 regular cells 3 — in 5 to 6 regular cells

6



(C = Chicken.


R = Rabbit.


P = Plasma.


E = Embryo Extract.)


TABLE XVII (Continued)

The Development of Unfertilized Rabbit Ova in Culture. (From Pincus, 1930)


Age of Ova

(Hours AFTER Copulation)


13 15 13 35


(11)

(12)

13 14

50

(13)

14

35

(14)

15



(15)

15

15

(16)

16



(17)

17

10

(18)

17

33

(19)

17

45


Number


Medium


RPCE RPRE

RPRE


RPRE RPCE


CPCE


RPRE


RPCE


RPCE


CPCE RPCE


Examined (Hours IN Culture)


47


43


25

27


30


27


22


23


48 26


Description


2 — unsegmented 1—16 to 20 cells 1 — in 2 cells and 2 to

5 polar bodies 3 — with about 5 polar

bodies 7 — unsegmented 2 — unsegmented 1 — in 4 regular cells

and 2 polar bodies 1 — in morula 1 — unsegmented 2 — in 3 regular cells 2 — in 4 regular cells 2— in 36 to 40 regular

cells 2 — in about 4 cells

regular 1 — with multiple polar

bodies 1 — unsegmented 1 — in 4 regular cells 1 — in about 16 cells 2 — in 1 very large cell

and 10 to 12 small

ones 2 — in about 16 cells 1— in 32 to 48 cells 1 — in 2 regular cells

and 2 polar bodies 1 — in 3 to 4 large

cells and 10 small

cells 1 — in 1 large cell and 16 small cells 2 — no segmentation 1 — 2 large, 2 small

cells and several

polar bodies 1 — in 16 very regular

cells 2— in 20 to 32 cells


Number Divided


Number Undivided


(C = Chicken.


R = Rabbit.


P = Plasma.


E = Embryo Extract.)


TABLE XVII (Continued)

The Development of Unfertilized Rabbit Ova in Culture.

Pincus, 1930)


(From


(20)


(21)


(22) (23)


(24) (25) (26)


(27)


(28)


Age of Ova

(Hours AFTER Copulation


18 10


18 li


18 20 18 25


18 30

18 50

19 5


19 30


19 45


Number


Medium


RPCE


RPCE


CPCE RPCE


RPRE RPRE RPCE


RPCE


RPCE


Examined

(Hours IN Culture)


48


29


47 24


48 47 22


27


22


Description


3 — unsegmented

1 — 2 unequal cells and

7 to 8 polar bodies 1 — 3 cells and several

polar bodies 1 — 4 regular cells 1 — 10 small cells and

1 large cell

4 — unsegmented

1 — 3 cells regular

2 — about 4 regular

cells, but shrunken 1 — in 12 regular cells 1 — in about 8 cells,

but shrunken 1 — unsegmented 1 — 3 polar bodies 2 — unsegmented 1 — 1 large cell and 2

to 3 small cells 1 — 2 regular cells and

2 polar bodies 1 — 4 regular cells 1 — 7 regular cells 4 — about 8 cells 2 — unsegmented

1 — in 3 cells

2 — in 8 regular cells

1 — in 10 regular cells

2 — unsegmented

2 — in 2 regular cells

4 — in 4 regular cells

1 — in 7 cells

1 — 2 unequal cells and

3 polar bodies 1 — unsegmented 1 — 2 regular cells 2 — 4 regular cells 1 — unsegmented 3— in 2 cells

2 — in 4 cells 1 — in 6 cells 1 — in 8 cells


Number Di

VIDEO


1(?)

8


Number Undivided


(C = Chicken


R = Rabbit.


P = Plasma.


E = Embryo Extract.)



The Development of


TABLE XVII (Continued)

Unfertilized Rabbit Ova Pincus, 1930)


IN Culture. (From



Age of Ova



Exam



Num


(Hours after Cop

Number

Medium

ined (Hours IN Cul

Description

Number Divided

ber Undi


ulation )



ture)



vided

(29)

20



2

CPCE

22

2 — many polar bodies

2



(30)

20

10

3

RPRE

49

3 — in many cells

3



(31)

20

20

4

RPCE

47

4 — unsegmented



4

(32)

20

20

2

CPCE

48

1 — unsegmented 1—1 large and 2 to 3 small cells

1

1

(33)

24

25

5

RPCE

27

1 — 2 unequal cells 3—2 regular cells 1 — 3 regular cells

5



(34)

24

45

2

RPRE

44

1 — 1 large cell and several polar bodies

1—16 to 20 regular cells and a few polar bodies

2



(35)

27

35

5

CPCE

46

1 — unsegmented 2 — about 8 cells and many polar bodies 2 — one large cell and many polar bodies

4

1

(36)

28

35

9

RPCE

47

4 — unsegment ed 1 — 4 regular cells 1 — 6 unequal cells 3— about 8 cells

5

4

(37)

37

20

2

RCPCE

27

2 — in many cells and degenerate

2



(38)

40

40

3

CPCE

45

3 — in many small cells

3



(39)

43

10

6

CPCE

46

1— in 2 cells

1 — in 4 cells and many

polar bodies 2 — in 1 cell and many

polar bodies 2 — in many small cells

6



(40)

47

30

6

RPCE

22

3 — unsegmented 1 — in 2 unequal cells 2 — with many polar bodies

3

3

(41)

48

30

8

RPCE

48

5 — unsegmented 3 — with many polar bodies

3

5

(42)

48

47

6

RPRE

52

1 — about 8 large cells

1 — 3 unequal cells and

many polar bodies

6



(C = Chicken.


R = Rabbit.


P = Plasma.


E = Embryo Extract.)


TABLE XVII (Continued)

The Development of Unfertilized Rabbit Ova in Culture. (From

Pincus, 1930)



Age of Ova

(Hours AFTER Copulation)

Number

Medium

Examined (Hours in Culture)

Description

Number Divided

Number Undivided



4— with many polar bodies



(43) (44) (45)

50 30 68 33

72

5 3

4

RPRE RPRE RPCE

45 45 22

1 — unsegmented

4 — in many cells

3— unsegmented and degenerate

2 — unsegmented and shrunken

2 — about 10 polar bodies and shrunken

4

2

1

3 2

(46)

73 40

7

RPCE

45

4 — unsegmented 2—16 regular (?) cells 1 — 5 cells and 3 polar bodies

3

4

(47)

96 45

2

RPCE

46

2— unsegmented



2


(C = Chicken.


R = Rabbit.


Plasma.


E = Embryo Extract.)


The primary and surprising fact evident from the data is that a majority of the ova placed in culture underwent a certain degree of development, so that out of 213 eggs cultured, 136 or 63.8 per cent are classified as having ^^ divided," the term ^'divided" including any degree of observable development beyond the 1 -celled state of the ova as recovered from the animals. It was the primary objective of these investigations to ascertain the nature of the various degrees of development undergone in vitro and to establish any relationship that might exist between the age of the ova and the nature of the development. Before undertaking any detailed analysis of the data it is deemed advisable to describe the various types of development observed.



Plate VIII

Ova from sterile matings as they appeared after being cultured in vitro. (From the Proceedings of the Royal Society.)


Recovered at 18 hrs.

Recovered at 27 hrs.

Recovered at 19 hrs.

Recovered at 18 hrs.

Recovered at 18 hrs.

Recovered at 19 hrs. Fig. 7, Recovered at 19 hrs. Fig. 8, Recovered at 28 hrs. Fig. 9, Recovered at 17 hrs. Fig. 10, Recovered at 24 hrs.


Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6,


30 mins.

30 mins.

5 mins.

10 mins,

15 mins

5 mins.

5 mins.

35 mins.

10 mins,

45 mins. after sterile copulation cultured for Fig. 11, Recovered at 37 hrs. after sterile copulation cultured for 6 hrs. Fig. covered at 73 hrs. 40 mins. after sterile copulation cultured for 45 hrs. Fig. covered at 73 hrs. 40 mins. after sterile copulation cultured for 45 hrs. Fig. covered from the ovary, and cultured for 28 hrs. Fig. 15, Recovered at 30 mins. after sterile copulation cultured for 24 hrs.


after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for after sterile copulation cultured for


44 hrs. 25 hrs. 22 hrs. 17 hrs. 28 hrs. 22 hrs.

22 hrs.

23 hrs.

23 hrs.

24 hrs.

12, Re 13, Re 14, Re48 hrs.


The ova observed in the 2-cell stage varied in appearance as shown in Plate VIII, Figs. 1-3. The great majority of them resembled that of Figure 1, and showed usually one, sometimes two or three, polar bodies. The ovum of Figure 3 was photographed after the egg had been in culture 22 hours. It was subsequently replaced, and when examined 24 hours later had formed eight cells quite regular in appearance. Note is made of this fact because it indicates that ova segmenting irregularly at the first division may eventually assume an appearance characteristic of ova undergoing quite regular division. The ovum of Figure 4 was photographed just as segmentation from two to three cells was being completed. One of the two blastomeres had not quite rounded out at the time of photographing. The segmented ovum of Figure 5 is also in three cells. When first examined after 23 hours of culturing no segmentation had occurred; 5 hours later the ovum had divided as photographed. The ova of Figure 5 were recovered at 18 hours and 15 minutes after copulation and were still surrounded by a number of follicle cells. They were placed vis-a-vis in culture and the out-growing follicle cells of each ovum became intermingled and caused the compression of the ova seen in the photograph. Figure 6 is a photograph of a typical 4-celled stage, exactly comparable to the 4-celled stage of fertilized ova (see Plate VII, Figs. 10 and 11). The number of polar bodies in such ova vary from one to three. Again, the great majority of ova observed in four cells presented the regular appearance of the ovum of Figure 6. Figure 7 represents an ovum containing seven cells in which one of the four blastomeres of the 4-celled stage divided twice while the others remained quiescent. Such differential division may begin after the 2-celled stage as illustrated by Figure 8, in which one of the original two cells has remained quiescent while the other divided in two, and one of the two cells formed divided twice to form four small cells. There is also photographed the single polar body of this ovum. Figure 9 represents another case in which one of the early blastomeres has remained quiescent while the others have gone on dividing at a rapid rate. Some such process is responsible for most of the irregular segmentations observed. At the same time segmentation may proceed in a manner comparable to that of normal fertilized ova in vivo, so that one may observe in the same culture the different types described. Figure 10 is a photograph of an ovum segmented to about 20 cells and apparently with a marked degree of regularity. When we come to consider ova segmented into 20 and more cells the interpretation of the course of their development becomes difficult because of a peculiar complication. The o\aim of Figure 11 offers a pertinent illustration. It w^as recovered from the tubes at 37 hours after copulation and was in the 1-cell stage. Six hours later it presented the appearance shown in the photograph. It has apparently segmented into about 36 cells in the course of 6 hours. This means astonishingly rapid segmentation. As a matter of fact what probably occurred was a complex fragmentation of the entire ovum. In the course of filming an ovum recovered at 29 hours and 20 minutes after copulation the course of such fragmentation was observed. After an initial period of quiescence the ovum underwent a period of activity which resulted in the sudden appearance of many small ^^ blast omeres." This was followed by a complete quiescence with the cessation of all cytoplasmic movements. The cells" of this fragmented ovum, however, were not at all distinct in form or outline. One may observe many-celled" ova. in culture that presented this vagueness of cell outline, but we have also seen well advanced ova in which the component blastomeres were as distinct and clear as in the normal fertilized ovum. Interpretation must, therefore, proceed slowly until the exact mechanics of division in vitro is thoroughly investigated. A certain amount of light, however, is shed on the problem by the consideration given below to the relation between the age of the ova and the nature of the development observed. Figures 12 and 13 are photographs of two ova recovered at 73 hours and 40 minutes after copulation. They were photographed after having been 45 hours in the same culture. Note the remarkable regularity of the cells of the ovum of Figure 13. The ova of Figures 14 and 15 represent types ordinarily described as "with many polar bodies." Both have a very large single cell, beside which lie a number of very small cells" comparable in appearance to polar bodies. Very often this group of polar bodies" resembles an irregular indented cytoplasmic mass, and I have actually seen it formed as such a mass budded or divided off from the main body of the cell. This represents the extreme of irregularity observed.

The foregoing account has been given irrespective of the age of the ova figured. It remains for us to ascertain if any relation does exist between the age of the ova cultured and the nature of their development. Before proceeding to a detailed inquiry, however, it must be pointed out that the various types of ova described and figured in the photographs have been observed in ova of all ages so that no absolute correlation exists. Ova have been considered as segmenting regularly only when the cells of the two, four, eight and sixteen cell stages have been of equal size, or when one could obviously trace the regular descent of the cells in ova exhibiting intermediate stages. In the cases of ova exhibiting many cells only those showing clear cell outlines and cells of equal size have been classified as "regular."


TABLE XVIII

Effect of Age of Ova when Removed from Doe on Subsequent Regularity of Division in Vitro. (From Pincus, 1930)


Group Number

Age of Ova (Hours after Copulation)

Regular

Irregular

Percentage Regular

(1) (2) (3)

11 to 17 17 to 21 24 to 96 All ova

26 37

10(?) 73

8 16 26 50

76.4 69.8 27.7 59.3


In Table XVIII the data are collected into three groups as follows: (1) Ova recovered when practically all were in the cumulus mass; (2) ova separating out of cumulus mass and not yet covered with albumen ; (3) ova covered with the albumen deposit. It is obvious from these data that the percentage of ova segmenting with any semblance of regularity decreased perceptibly with the age of the ova. In the group of ova recovered at 24 to 96 hours after copulation 16 of the ova classified as irregular exhibited one large cell and many polar bodies." In fact, 23 or about half of all the ova called irregular" are of this type. A number of ova, particularly in the 24 to 96 hour group exhibited "many polar bodies" and a varying number of larger cells. The rest of the ova classified as irregular were either "manycelled" with indistinct cell outlines, or contained cells of unequal size traceable, probably, to the differential division of early blastomeres.


Now this fact that the younger ova tend to segment regularly is presumably related to the state of the egg cytoplasm. The older ova undoubtedly undergo a certain degree of degeneration as they progress down the tubes, and the degree of cytoplasmic degeneration is probably related to the regularity of the subsequent development in culture. The problem is unfortunately complicated by the fact that all ova in culture stop segmenting and degenerate after some time. In these experiments it is probable that practically no development occurs after the ova have been in culture for 36 hours. The time in which the ova may exhibit their potentialities for parthenogenetic development is, under the conditions of these experiments, therefore extremely limited. The surprising fact is that such a large proportion of the ova do exhibit a degree of development that must be classified as parthenogenetic.


The morphology and cytology of parthenogenetic ova have been studied in a number of invertebrate forms where parthenogenetic development has been induced by various methods of treatment. In almost all cases a very large proportion of the parthenogenetic ova exhibit marked irregularities in development {e.g., Wilson, 1901; Scott, 1906; Morris, 1917). In fact all the irregular types described here have been observed in artificially parthenogenetic invertebrate ova. The proportion of regular divisions observed in these ova compares favorably with those observed in invertebrate ova, with the possible exception of the seaurchin eggs, a very large proportion of which (as much as 100 per cent) may develop regularly into swinaming larvae (Hindle, 1910; Loeb, 1913).


It was not possible to make any extensive cytological study of the ova described. The few sectioned and stained eggs obtained, indicate that in ova segmenting regularly the nuclei and cytoplasm are normal in appearance. In ova segmenting irregularly the situation is apparently rather comphcated. There are obvious evidences of degeneration. Some cells contain nuclei, others do not, and the cytoplasm is often quite degenerate. One observes ova with several nuclei and no distinct cell divisions. In the case of one fairly regular ovum there were at least 37 chromosomes in an incomplete metaphase plate.


Upon consideration of the various factors involved in the technique of explanting the ova it seemed most likely that those young ova which underwent a normal parthenogenetic cleavage were stimulated by a gradually developed hypertonicity of the culture medium. For in these experiments the ova were cultured in watch glasses in a moist chamber, where the evaporation of a small amount of water from the plasma culture was possible. If this conclusion is true then at least one of the many types of parthenogenetic stimuli known to be effective with non-mammalian ova is similarly stimulating to mammalian eggs.


In order to examine this question further the writer and Dr. E. V. Enzmann (Pincus and Enzmann, 1936a) have studied the effect of known methods of parthenogenetic stimulation upon rabbit ova. We took as our criterion of activation the production of the second polar body, which, as we have seen in the experiments with semination in vitro, is entirely adequate.


The data of these experiments are given in Table XIX. They demonstrate that short treatment with solutions of relatively low hypertonicity are certainly effective in in


TABLE XIX

The Effect of Various Treatments upon the Activation of Rabbit Ova IX Vitro. (From the Journal of Experimental Zoology)


Date


18/1/34


24/1/34


24/1/34


24/1/34


20/IX/35

20/IX/35

21/IX/35 21/IX/35

21/IX/35

20/IX/35 20/IX/35 21/IX/35 21/IX/35

18/IX/35


Treatment


3 minutes in 2.8 c.c. H/10 butyric acid + 50 c.c. Ringer-Locke followed by 3 mins. in 8 c.c. 2.5% NaCl -f 50 c.c. Ringer-Locke followed by plasma culture

3 minutes in 5 c.c. N/10 butyric acid -f 100 c.c. Ringer-Locke followed by hypertonic solution as above

3 minutes in 7.5 c.c. N/10 butyric acid -|- 100 c.c. Ringer-Locke followed by hypertonic solution as above

3 minutes in 10 c.c. N/10 butyric acid -]- 100 c.c. Ringer-Locke followed by hypertonic solution as above

10 minutes in 1.8% Ringer-Locke

5 minutes in 1.8% Ringer-Locke

8 minutes in 1.8% Ringer-Locke 8 minutes in 1.6% Ringer-Locke

8 minutes in 2.0% Ringer-Locke

2 minutes exposure to 45.5° C.

3 minutes exposure to 45.5° C. 2^ minutes exposure to 45.5° C. 3 minutes exposure to 45.5° C.

2 minutes exposure to 60° C.


Result


Cumulus partly dispersed ; one ovum with 2 polar bodies; 7 with 1 polar body; much shrinkage

Cumulus partly dispersed; 2 ova with 2 polar bodies; with 1 polar body; much shrinkage

Plasmolysis of ova


Plasmolysis of ova


Cumulus intact; only 1st polar

body Cumulus intact; only 1st polar

body 3 polar bodies in 5 hours

1 egg with 2 polar bodies; 1 egg with 3 polar bodies

2 polar bodies in 3 hours 3^ with 2 polar bodies

2 or 3 polar bodies per egg 2 polar bodies formed 2 or 3 polar bodies per egg No polar body formation


ducing activation, and that more drastic treatment (e.g., longer treatment, or Loeb's treatment) is only occasionally effective. This indicates that the optimum conditions for the activation of rabbit ova are different from those employed with sea-urchin eggs. - The data on the experiments with ova heated to 45° to 47° show that this heat treatment is most effectively activating.


We may conclude therefore that certain of the methods ordinarily employed in the artificial activation of nonmammalian ova are also effective in activating mammalian eggs. In a preliminary group of experiments (unpublished data) the writer has transplanted ova so activated into the fallopian tubes of pseudopregnant rabbit does and has later recovered the transplanted ova. A number had undergone normal but obviously belated cleavage. A few cleaved at the normal rate and about 10% of the total attained the blastula stage.


In order to obviate any undetected effects of the manipulation of ova in vitro Pincus and Enzmann (1936a) undertook the activation of ova in vivo by injecting into the tops of rabbit fallopian tubes sperm suspensions previously irradiated with ultraviolet light of 2357 A° wavelength. The does used in these experiments had been mated to sterile bucks 12 to 13 hours previously so that their ovulated ova were embedded in the follicle cell plug. Into one oviduct the rayed sperm were injected, into the other an identical sample of unrayed sperm. It was found that ova from the tubes receiving unrayed sperm suspensions were for the most part normally fertilized and cleaved at the normal rate. Ova seminated with rayed sperm showed varying proportions of normally cleavage stages depending upon the time of exposure of the sperm to the ultraviolet light. Long exposures resulted in a preponderance of irregularly cleaved ova. But even the regularly cleaved ova resulting from seminations of sperm given short exposures were markedly retarded when compared with the control ova in the other tube.


The ultraviolet treatment with the particular wavelength used results presumably in the inactivation of the sperm chromatin (see Swann and del Rosario, 1932), and depending on the time of exposure (e.g., intensity of radiation) leaves the non-chromatic portions of the sperm relatively unaffected. Dalq and Simon (1931) have shown that sperm treated with ultraviolet light penetrate into the egg cytoplasm but pronucleus formation does not occur and the chromatin disintegrates. If the sperm centrosome apparatus is not inactivated normal cleavage occurs, otherwise irregular development ensues.


The data of Pincus (1930) indicate that parthenogenetic cleavages occur later than normal cleavages (although the time taken for the segmentation process itself is the same in fertilized and unfertilized eggs) . It thus appears that the retarded cleavages observed in vivo as the result of semination with irradiated sperm are parthenogenetic in the sense that the sperm chromatin did not participate in the mitoses.


Novak and Eisinger (1923) attempted to activate rabbit eggs by tying off the tubes at the isthmus to prevent entry of the ova into the uterus. The ova that they recovered were either irregularly cleaved or fragmented with perhaps one or two normal cleavages. Their data thus resemble those of Mann (1924) on rat ova (see Table VIII) which do not descend into the uterus in unmated animals. Grusdew (1896) who injected sperm into the tops of rabbit tubes together with ova from punctured follicles also tied the tubes off at the isthmus and in a number of ova which gave no evidence of sperm penetration he observed ordinarily irregular but occasionally regular development. It would seem then that parthenogenetic development may be induced in vivo but that extensive embryonic differentiation has not been demonstrated.


It is obvious, of course, that a mere beginning has been made in the investigation of the parthenogenetic potencies of tubal ova. Presumably normal embryos might develop if a diploid cleavage nucleus could be induced to form. Pincus and Enzmann (1935) have, in fact, found indications that such a process may occur in activated rabbit eggs noting, again, after a rather long latent period, two fusion nuclei in unfertilized ova. The writer has observed an initial nuclear division without cytoplasmic cleavage in a primate ovarian ovum cultured t/i vitro. For full development in vivo it seems necessary that parthenogenetic ova should duplicate with some exactitude not only the normal morphological changes but also the rate of these processes. For the differentiating embryo is dependent upon an uterine environment the optimum development of which involves a fairly definite time schedule.



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Pincus G. The Eggs of Mammals. (1936) The Macmillan Company, New York.

Historic Disclaimer - information about historic embryology pages 
Mark Hill.jpg
Pages where the terms "Historic" (textbooks, papers, people, recommendations) 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, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Eggs of Mammals

The Eggs of Mammals (1936): Introduction | The Origin of the Definitive Ova | The Growth of the Ovum | The Development and Atresia of Full-Grown Ova and the Problem of Ovarian Parthenogenesis | Methods Employed in the Experimental Manipulation of Mammalian Ova | The Tubal History of Unfertilized Eggs | Fertilization and Cleavage | The Activation of Unfertilized Eggs | The Growth and Implantation of the Blastodermic Vesicle | Summary and Recapitulation | Bibliography | Figures | Historic Disclaimer

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