Book - Outline of Comparative Embryology 1-4

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Richards A Outline of Comparative Embryology. (1931)
1931 Richards: Part One General Embryology 1 Historical Development of Embryology | 2 The Germ-Cell Cycle | 3 Egg and Cleavage Types | 4 Holoblastic Types of Cleavage | 5 Meroblastic Types of Cleavage | 6 Types of Blastulae | 7 Endoderm Formation | 8 Mesoderm Formation | 9 Types of Invertebrate Larvae | 10 Formation of the Mammalian Embryo | 11 Egg and Embryonic Membranes | Part Two Embryological Problems 1 The Origin And Development Of Germ Cells | 2 Germ-Layer Theory | 3 The Recapitulation Theory | 4 Asexual Reproduction | 5 Parthenogenesis | 6 Paedogenesis And Neoteny | 7 Polyembryony | 8 The Determination Problem | 9 Ecological Control Of Invertebrate Larval Types

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This historic 1931 embryology textbook by Richards was designed as an introduction to the topic. Currently only the text has been made available online, figures will be added at a later date. My thanks to the Internet Archive for making the original scanned book available.
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Part One General Embryology

Chapter IV Holoblastic Types of Cleavage

I. Radial Cleavage

The eggs of the Porifera, of all the coelenterates, except the ctenophores, and of the echinoderrns have radial cleavage. Formerly amphioxus was given as a type of this class, but it has been shown that the older accounts were in error, and that its cleavage is really bilateral.


Fig. 10. The vleiivage of sea cucumber Synapta dig/Lluta. (Redrawn from horsehclt and Heider after Selcnka.)

A. 2-cell stage; B, polar View of 4-cell stage; C, D, lateral views of 8- and 16—cell stages.

Radial cleavage includes eggs of both homolecithal and teloleeithal types, although of the latter of course only those which have holoblastie cleavage belong here. In the typical and simple cases such as that of Synapta (which as described by Selenka may be taken as most nearly

corresponding to the ideal form of radial cleavage), the division planes 28 RADIAL CLEAVAGE 29

succeed each other in regular alternation dividing the egg first meridionally and then equatorially into equal blastomeres. It very nearly cor— responds to the Sachs’ principle of the alternation at right angles of successive planes of cell division. The first furrow is meridional and divides the egg equally. The second furrow is also meridional and

1 It: 11 Continuation of fig 10 32-, 64-, and 128-cell st Lges of S:/napta dmztata

divides each of the first two blastomeres equally. The third furrow is equatorial and the blastomeres are equal, making eight cells arranged in two rows about the two poles. By this time a tiny cavity is discoverable at the center of the mass which is to become the cleavage cavity or blastocoele. The furrows of the next cleavage are meridional but at an angle of 45 degrees to the first and second. The furrows of the fifth are again latitudinal, dividing all the blastomeres equally. Subsequently the divisions keep their regular alternation for a period, forming a blastula in which the cells are arranged in horizontal and vertical rows. With 2 shift of the blastomeres about the pole by which the opening there is closed, a spherical blastula consisting of a single layer of cells (a typical coeloblastula) is formed.

The cleavage of many jellyfishes, though in general radial, undergoes many modifications due to yolk distribution, loose arrangement of cells, and to other factors.

Radial cleavage undergoes some interesting modifications in some of the sea-urchins, notably Strongylocentrotus lividus, as shown by Boveri (1901). In this form cleavage is unequal and differential. The egg is of a clearly determinative type, a jelly canal indicating the position in which the polar bodies will be given Off. It is the place at which, in the oocyte stage, there is uniformly distributed an orange—yellow pigment which, upon fertilization of the egg, at once rearranges itself as a band about the lower half of the egg, leaving a cap without pigment about the vegetal pole. This cap is destined to produce in subsequent cleavages small cells known as inicromcres, a phenomenon which in itself is striking since in most eggs the cells at the vegetative pole are commonly larger than those of the animal half. The egg nucleus is not limited to the animal half of the egg, nor is the spermatozoon restricted to the jelly canal.

The first two cleavages are meridional and equal, resulting in foul blastomeres which receive equal amounts of the three kinds of egg materials, the pigment—free animal half, the pigment zone, and the clear polar cap. With the next cleavage which is nearly equal (latitudinal) the four animal blastomeres receive but a small portion of the pigment, the remainder being in the four blastomeres of the vegetal half of the egg. Now follows a peculiar differential cleavage, the upper four cells dividing meridionally while the lower four are unequally divided latitudinally. This results in the immediate segregation of the pigment-free cap into four vegetative cells, the micromeres. The descendants of these are later to form the primary mesoderm.

In producing the next stage (32 cells) the eight cells of the animal half (mesomeres) divide equally and latitudinally producing two wreaths of eight cells each. The four larger pigmented macromcres divide meridionally, and the four micromeres of the unpigmented cap latitudina.lly and unequally. Subsequent divisions tend to equalize the size differences and the blastula is regular and consists of equal—sized cells, but from the substance of the mesomeres comes the ectoderm, except that of the lower pigmented area which is contributed to the secondary mesoderm; from the macromeres come the endoderm and secondary mesoderm; and the primary mesoderm is from the micromeres. fiG 1! (‘tonvage of sea.-urchm Strormylorerwrotm (Rcdnuvn from Korschelt and Hmder after Boven )

Lateral vlesw shmx 1212. Lhe three zones and their dxsmbutxon 1n the blastomerea

II. Disymmetrical Cleavage

The ctenophores are the sole representatives of the disymmetrical type of cleavage, and to the average student of embryology the fact that they constitute a remarkable exception to the general rules is their greatest interest. Although the peculiarities of these forms early stimulated a great deal of investigation, Ziegler’s findings (1898) form the basis of our present understanding of this type of development. DISYMMETRICAL CLEAVAGE 33


Fig. 13. Cleavage of Baron. (Rcdruwn from Korsclu-It and Heidcr after Zoigler.)

A. second division. The vegetative pole is the upper, as in other figure showing lateral view; B. 4-cell stage; C, 8-cell stage from animal pole, as, median plane; bl), transverse plane; D. same from lateral view; E, F, 16—cell stages from animal pole and from side View respectively.


The eggs of ctenophores have an ectoplasmic surface layer and an inner vaeuolated yolk mass; the nucleus lies in the ectoplasm near the vegetative pole of the egg where the polar bodies are given off (Hatschek). In no other case in the animal kingdom is this type of egg organization found. The first and second cleavage furrows begin at the vegetative pole, advancing meridionally to the animal pole, dividing the egg equally. The first furrow corresponds to the median plane of the adult and the second to a plane connecting the two long tentacles; each blastomere is therefore one-fourth (one quadrant) of the body.

The third division is spoken of as diagonal. It runs obliquely from near the animal pole to the lateral part of the vegetative half of the egg,


Fig. 14. A, continuation of fig. 13. 40~('ell stage of Iftrut; B, g.-1-«it|ul.r of ('ulluum4L bialnta. (After Metelmlkoff.)

er. outer cells, eetoderm; en. large inner cells, endoderni; in. small inner cells, niesoderm

giving rise to a curved plate of eight cells of which the four larger middle ones are called submedian and the four somewhat smaller ones are the subtentacular cells. This curved plate, concave on the animal side, is thus divided symmetrically in two directions, but is elongated in the tentacle plane, thus giving the impression that there are two centers of symmetry, one in each half, right and left, of the embryo. This impression is accentuated in the next stage in which eight micromeres in two distinct groups are given off on the concave side (animal half) of the embryo. The 32-cell stage is reached as each of the eight macromeres gives off another micromere and each of the old micromeres divides. The micromeres of the submedian octants divide equally, those of the subtentacular ones very unequally.

By subsequent divisions the micromeres come to form an ectodermal cap which gradually grows over the macromeres. now increased to 16.


The cap of ectomeres closes up late at the animal pole, a point at whit.-. the sense organ later develops. In the formation of the eetodermal cap of micromeres gastrulation is accomplished and the endoderm is marked off from the eetoderm. Endoderm formation in the animal kingdom may be accomplished by several methods which are described in Chapter VII. Although invagination is the most common of these methods it is by no means a necessary process in endoderm formation. In this case it plays no part at all, for the large maeromeres that are the primordia of the endoderni are simply overgrown by the micromeres. This process is known as epiboly. The epibolic gastrula of Callianira is shown in fig. 14B. For further details in the development of ctenophores the student is referred to the descriptions of Ziegler, Metchnikoff, and others.

III. Bilateral Cleavage

Bilateral cleavage is so called because of a bilateral arrangement of the egg substances which is very often recognizable before cleavage, indeed before fertilization in some cases, and certainly early in cleavage. Examples include rotifers, nematodes. and those vertebrates which have holoblastic cleavage. Thus it occurs in eggs which belong to homolecithal and to holoblastic teloleeithal types, and either equal or decidedly unequal cleavage may result. It will be recalled that telolecithal eggs may have holoblastic or meroblastic cleavage depending on the degree in which the yolk mass forces the cytoplasm to be localized on one side. In the extreme cases discoidal cleavage results, which is thus related to the bilateral types. On the other hand it will later appear that the discoidal type is also related to the superficial type.

1 . Amphioxus

As a first type amphioxus may be chosen. It was formerly the custom to class amphioxus as of the radial type. This is perhaps to be ascribed to the fact that there is some variability in the behavior of different eggs. Cerfontaine carefully restudied the case, however (1906), and found that in the majority of cases the following description holds true. Since his work, nevertheless, it should perhaps be pointed out, as Dean has done, that the cleavage of amphioxus may be polymorphic, that is, in one case radial and in another bilateral.

The egg of amphioxus is clearly bilateral in structure before cleavage. The animal pole is marked by the second polar body, the first being given off before the formation of the vitelline membrane and so lost. It is said that the animal pole is the point of attachment of the oocyte to the germinal epithelium. If the egg is oriented according to the planes of the future embryo the animal pole is found to be in the center of the AMI’HI()XI'S 35

antcro-ventral iegion and the vegetal in that of the postei'o—dorsu.l. In the anterior half of the egg may be distinguished a clear mass of yolk-free cytoplasm, in which the nucleus lies, although part of this mass extends a little into the posterior half on the ventral side; most of the cytoplasm of the posterior half of the egg is well filled with yolk globules. Yolk granules also are found in the animal half outside the clear cytoplasmic area. The distinction of yolk-free and yolk-laden halves of the egg is indicative of its bilateral symmetry. The telolecithal character of the egg is peculiar in that the yolk mass is not only in the vegetative half, but toward the


Tie 15 Median section through egg of amphioxus arranged to show relation of egg AXIS to future orientation of body (After (‘erfoiit.iine)

.in -\ egg ‘LXIS terniiimtiiig in the two poles, A, P l), V, the future dlll(‘l‘10I‘, posterior, dors ll and Ventral I‘('§Il01I\ of the egg

posterior end. The first furrow is meridional and corresponds to the median plane, dividing the egg into right and left halves. The second furrow is meridional, but slightly unequal blastoineres are separated by it. The antero-dorsal are the smaller. The third furrow is latitudinal, cutting off four micromeres at the animal pole. Owing to the inequality of the 4-cell stage there are really four pairs of cells of different sizes in the 8-cell stage.

The 16-cell stage is not reached by meridional furrows as is to be expected. The four micromeres each divide by a furrow more or less at right angles to the median plane, and the four macromei-es by a parallel furrow. Thus there arise two plates of eight cells each, those of the animal half curving from front to back, while the others curve from right to left.

From this stage on, development becomes irregular, and characteristic differentlations appear. The typical coeloblastula characteristic of

P10. 16 Cleavage of amphioxus (Redrawn from Korschelt and Herder, after Cerfontame)

A, second cleavage, B, 4—cell stage from left side C, D, 8-cell stage from side view and from animal pole

amphioxus is formed with smaller ectoderm—producing cells at the animal pole and the larger endoderm-forming ones at the vegetative. By invagination, epiboly, and involution the gastrula is formed.

2. Ascidians

The bilateral cleavage of the ascidians has been studied by many embryologists, but Conklin’s work on Cynthza, Cwna, and Mogula IS E f 16-cell stage 111 left sxde

0 um 3. mm. H mm nb EC Lu BM mh aL .0. E] S e V 1 6|.‘ 8 38 HOLOBLASTIC TYPES OF CLEAVAGE

probably the most complete. These eggs have typical determinative cleavage, with definite orrgamforming regions which are recognizable by «color difference of the cytoplasm.

The newly extruded egg surrounded by a layer of test has a conical layer of texoplasm in which is uniformly distributed a yellow pigment. Soon after fertilization the polar bodies are given off and peculiar rearrangements of substance take place. About five minutes after fertiliza


fiG. 15. The egg of Cynthia partzta. (After Conklm.)

A. unfertilized em: with germinal vesicle, central gray yolk 111.158, peripheral yellow protoplasm, and test cells; B, five minutes after fertilization showing streaming of yellow protoplasm to vegetative pole; (‘, streaming of yellow protoplasm nearly completed, clear protoplasm lies beneath it and is visible at its upper edge. On the top of the cm: the germinal vesicle is still seen; D, the light creseentic area at the vegetative pole represents the male pronueleus; the unstippled area is the gray central yolk mass of A; E, polyspermic egg: F. formation of yellow crescent (heavily stippled) with the light gray trescent above it.

tion the yellow pigment, mesoplasm, may be seen streaming toward the vegetal pole, leaving behind the gray yolk mass, endoplasm, which fills most of the cytoplasm of the egg. The yellow mesoplasm arranges itself in a crescent in the posterior half and will, later in development, give rise to mesoderm. The large germinal vesicle contains material in addition to that which goes to form the cleavage nucleus, which is liberated at the time of formation of the maturation spindle. This material, the clear protoplasm, is the ectoplasm of the fertilized egg; it shifts its position to lie in a clear gray crescent next to the yellow crescent but on the side of Ab(.‘lDlAl\h .39)

the animal pole. It IS the neurochordal anlage (or fundainent from which will arise the neural canal and notochord). The animal pole is suiirounded by ectoplasm from which ectoderm arises, and the vegetative Iby endoplasm producing endoderm.

The first division, a meridional one, divides the egg and likewise each of the oigan-foiming rogiorns into «two equal halves Since tliere is but a

fiG 10 A, continuation of fig 18 B, showing aggregriiion of test cells over the crescent and the protrusion of the ehorion, (‘, 2-cell stage with formative substances outlined Uniform stipples, volk, light stipples, clear protoplisni eiilarged and extended toward the animal pole, grouped stipples, yellow crescent m Lterial

single plane which can do this it is evident that the cleavage is bilateral in character. The separation of the egg substance into organ—forming regions, which had started during the first cleavage, is completed now, although it must be recognized that it is never as sharp as the boundaries of the regions shown in_the usual diagrams. It is not possible, however, that living protoplasms could be entirely and sharply separated from each other while in a single cell. Indeed, we may regard the process of cleavage as having the especial function of distributing these substances into the appropriate cells.

The second division is meridional and displays the beginning of inequality. The orientation of the ascidian egg is similar to that of amphioxus. Therefore, two antero-dorsal cells are separated by this division from two postero—ventral ones. It is customary to designate the anterior cells by the letter A and the posterior by the letter B. In each case the right blastomere is indicated by underlining the letter

fiG. 20. Cleavage of Cynthia (Redmwn from Korschclt and H0|dOf, after Conklm )

A. 4-cell stage from left side, B, from animal pole, C‘, 8-coll stage from left side, I), from animal pole.

as 51} or E‘. The exponent 3 indicates that this is the third cell generation, counting the single-celled egg as 1. The division of A3 results in two blastomeres which are designated A‘ 1 and A4 2. The exponent 4 indicates the fourth cell generation, and the 1 or 2 after the period shows that it is the first or second cell from the vegetal pole. These principles of nomenclature are used throughout the cell lineage of the ascidian.

The third division is somewhat unequal and latitudinal, resulting in 4 cells of the animal half of the embryo (a”, b‘ 2, g4-2, lg‘-2) which are smaller than the corresponding ones of the vegetative half (A44, 51“, B‘ 1, Q‘ ‘). Due to a shift in the position of the spindles of the animal ASCIDIANS 41

half which converge toward the plane, the nuclei of a4 7 and Q” lie nearer to each other than do those of A4-7 and 44'”. We may take the A or the anterior half of the embryo as the type; the cells of the posterior half are to be regarded similarly.

The next division is therefore not strictly meridional as is to be expected. The spindles of the small animal cells (a‘‘-‘’, 9”) lie nearly parallel to the median plane, but those of the broader animal cells are more transversely placed. Thereupon the cells 115-3 and a5-4 seem to be behind each other, while 125-3 an(l I)“ are side by side. In the vegetative half the converse relations hold: A“ and A7’-7 lie side by side and B5-7


A B C fiG. ‘.21. Later stages of ('ymhia cleavage. (Redrawn from Korschelt and Heider, after Conklin.)

A, the fourth cleavage seen from animal pole; B, vegetative half of embryo in 32-cell stage; C. same in 64-cell stage.

A7 7, A7 7, B7 7, B7 7, are pure endoderm cells; A“ 7, A“ ‘, are cells of neuroehnrda anlage; B“ 7, B“ -'5, B" 4, mesoderm crescent; A7 G, A7 7, go to form the notochord; A7 '7. A7 ‘. form hinder part of neural plate. A7 " contains gray yolk (endoderm), but it eonmins material uhieh will be segregated as mesenehyme. B7 ‘, is muscle forming; B7 3 mesem-hyme. In each case the symmetrical mates of the left side have a similar fate.

and B5-7 lie behind one another. B” and half of B5-7 are the material from the yellow crescent. The left half is similar.

From here on all the cells of the animal half produce only eetoderm cells. The cells of the vegetative half are more diversely differentiated. B“-7 and Q“-7 consist only of yellow protoplasm and are purely mesodermal; A”, A“, and B“ with their mates of the right side are almost purely endodermal. The neurochordal cells A“ and A“ lie next to them anteriorly, and the crescentie mesoderm anlage, B”, B”, and B“, behind.

From this it will be seen without going into further details that the cleavage of the ascidians is a very good example of the determinative type. Thus organ-forming regions are definitely localized during the maturation and fertilization processes and by the process of cleavage 42 H()L()BLAS'l‘IC TYPES OF CLII«‘.AV.A'(:I«:

are segregated into definite cells from wvlficln arcise the organs of the lafterfembryo in the characteristic ascidian manner.

I 2 3 4 5 ‘5 Result U7) W0) W9) ‘K 19) ‘( 32*) l( 54» an I 3" ' ectoderm an A: A“ A‘-4 neurochordal A” endodermal , At! A” A” neurochordal A A‘-‘ endodermal ‘ an _¢_i_” { ectoderm 55.3 As — A53 33-4 neurochordal _ A‘-9 endodermal A4 I A“ A“ neurochordal Egg — A‘-‘ endodermal b5.4 b” { ectoderm has 33 35-! BM mesoder Be 3 m 34.1 B“ B‘-2 yellow protoplasm—mesodermal B B54 endodermal bu L‘-" { } ectoderm has is 5 4 .13.” %6'3 } mesoderm B4 1 -‘ B5‘, §__‘-’ yellow protoplasm " B“ endodermal


3. Vertebrates

The cleavage of the vertebrates is not usually of a determinative character as is that of the ascidians, and there are many variations in the characters it presents throughout the different groups. In general, however, they may all be referred to the bilateral type or derived from it, although the very considerable amounts of yolk present in the teloV lecithal eggs bring about important modifications in the modes of cleavage. This account leaves out of consideration the cleavage of mammals which is modified in an extreme manner in spite of the lack eofiyolk. Several groups of vertebrates have discoidal cleavage; this type,

fiG. ‘.32. Cleavage of the frog egg. A, B. C, D, 2-. 4-. 8-. 32—eell stages; E. lutor cleavage stage: 1“. dorsal lip of blastopore; G. circular blastoporc.

however, is joined to the holoblastic egg types by many transitional stages and types.

All amphibia have total, unequal cleavage in correlation with the telolecithal type of egg structure which characterizes this group. The egg of the frog has been studied by many investigators and may be taken as an example of holoblastic cleavage in the vertebrates. A dark 44 HOLOBLASTIC TYPES OF CLEAVAGE

brown or blackish pigment distinguishes the animal from the vegetative portions of the egg. About the vegetative pole extending perhaps onethird upwards is a white region which contains the material that will later go to form the endoderm.

In some form of amphibians, as of other groups, it is impossible to relate the cleavage planes to the later axes of symmetry of the embryo or larva. In other forms the bilateral arrangement of the blastomeres is unmistakable.


fiG 23 Cleavage of the frog egg seen from the animal or pigmented pole A. B, C. 4-, 8-, 32-cell stages

In the frog there is considerable variation as to the relations of the cleavage planes. Brachet found in 48 per cent of the cases which he observed that the first cleavage plane and the median plane coincided; in another 20 per cent the deviation was not more than 20 degrees. However, the bilaterality of the egg may often be shown to be independent of the cleavage figures. In certain amphibian eggs it has been shown that there is present in both fertilized and unfertilized eggs a bilateral arrangement of part of the egg substance, the so-called “gray crescent,” which appears at the edge of the white part of the egg against the dark portion, recalling the condition in ascidians.

The first cleavage divides the egg meridionally, the formation of the VER’l‘EBRA'l‘ES 45

furrow beginning at the animal pole and extending to the vegetal pole. The second is similar to the first but at right angles to it. The third cleavage is latitudinal and the blastomeres resulting form two circlets, one of four large cells and the other of four smaller. The fourth cleavages are meridional again. In later cleavages the yolk in the vegetative region causes a retardation in the rate of division so that the animal cells become much more numerous. In the fifth and sixth cleavages only the small

fiG. 24. Sections through blastulue up to the beginning of gastrulation in the frog“; egg. (B, (‘, D, after Ziegler) These show the clmracter of the octoderm and endoderm cells, the nature of the blastoeoelc, and the first sign of gastrular invagmation.

upper cirelets of cells are divided and even in those disturbances in the pattern of the blastomeres shortly appear. No longer is the wreath-like arrangement of the cells maintained and they become relatively smaller and much more numerous as compared with the large yolk-laden cells of the vegetal region.

The cleavage cavity which may be discerned in the 8-cell stage is smaller than that of almphioxus or the ascidian and is pushed toward the animal pole by the larger yolk cells. It gradually becomes more 46 HOLOBLASTIC TYPES OF CLEAVAGE

extended laterally, but in places it is reduced to a mere slit as development proceeds. When the fully formed blastula is reached in the frog, a difference, which is characteristic between vertebrates and invertebrates, becomes apparent in that the wall consists of many cells. In the invertebrates the octoderm and later the endoderm consist of a single layer of columnar or cuboidal epithelium, but in the vertebrates these germ layers are of several cells in thickness and many of the cells do not lie in contact with either the outer or inner surface.

4. Nematodes

The cleavage of nematodes may be illustrated by reference to the development of Ascaris worked out by Boveri; a number of other investigators have worked on other forms and have shown that they are in agreement with the Ascaris type.

The egg is small and practically yolk—free, and no evidences of differentiation are visible in the uncleaved egg, nor of relation between cleavage planes and polar bodies, but as soon as the 4-cell condition is reached the orientation is complete. In addition, however, to the differentiation which is expressed in the. orientation of the 4-cell stage, another mark of differentiation is evident in the nuclear processes. This is the chromatin diminution which occurs in the cells which are somatic in character, and is lacking in the prospective germ cell line, that is, in P1, P2, P3, P4, and G and G1.

The first cleavage plane results in the formation of two cells somewhat unequal. Of these the larger is designated as S1 01' AB and the smaller as P1. S, is shown by its subsequent development to contain only material which is to be distributed to somatic cells, while the P1 contains materials which will contribute to both soma and germ plasm. The next cleavage planes are not parallel to each other, for the spindle of the AB cell lies parallel to the first division plane, but that of the P1 cell is perpendicular to it. Thus there arises a T-shaped figure, the top being formed by the cells A and B and the stem at first by P1, which divides more slowly than the S1 cell, and later by the derivatives, cells S2 and Pa. Subsequently the P2 cell shifts posteriorly so that it comes to lie in contact with both S2 and B, forming a rhomboidal figure.

Now the bilateral character of the embryo becomes apparent. The cells A and B are dorsal, A being anterior; S2 and P2 are ventral, 83 being anterior. The dorsal cells now divide somewhat ahead of the ventral by a plane of cleavage which lies in the median line; A thus divides into a on the right side and 0: on the left, and B into b and 6. The embryo for a brief time, therefore, is in a 6-celled condition, but the division of the two ventral cells follows shortly, the planes of diviNEMATODES 47

sion lying perpendicular to the median plane. The 8-cell stage, therefore, consists of 9. plate of four dorsal ectomeres (two right and two left) and

flu. 2.3. (‘leuvage of Ascaris ntcgalocephala. (Rt.-drawn from Korschelt and Heider after Bovcri.)

A. 2-coll stage with spindles for the third cleavage; S; which equals AB is the first somatic cell and P1 is the blnstomoro from which the germ line will be segregated (stem cell); B. C‘, D, 4-celled stages showing in B the characteristic T-form resulting from the spindle directions of the second cleavage in C the Pa cell swinging around to form the characteristic rhomboidnl figure of the 4—cell stage. P2 is the stem cell.

8. row of four ventral cells slightly curved. S2 (EM St) divides into M St and E, the former being the anlage of mesoderm and stomodaeum and the latter that of the primitive endoderm. P2 divides into S3, an ectomesoderm cell, and P3, a continuation of the germ line. In this 8-cell stage the cleavage cavity makes its first appearance.

While the cleavage processes are taking place in Ascaris as described they are accompanied by nuclear changes of a character which has occasioned much study and discussion. In certain of the cells there occurs a process known as chromatin diminution by means of which

Fig. 26. Continuation of fig. 25.

A. 6-cell stage. Blastomcres A and B divided into a and a. and b and Li; B. 7-cell stage I’2 having divided into Pa and S3. A and B are seen from the right side; C‘, seen from the dorsal side; D, 8-cell stage. S2 having divided into E and MSt.

the thickened ends of the chromosomes are left behind in the cytoplasm as the telophases of the cleavage divisions take place. Chromatin diminution never occurs in those blastomeres which are antecedent to the germ cells of the later stages; but every blastomere which will produce only somatic cells goes through the process of chromatin diminution once. In the 2-cell stage S1 undergoes chromatin diminution while P1 does not. In the 4-cell stage S2 repeats the process but P2 does not. In NEMATODES 49

the 8-cell stage again P3 retains its entire chromatin complement while its sister cell S3 shows the differential loss. This setting aside of the germ

3 I a I‘ a,I‘ a H a II‘ 8 all’ A ad “P 0‘ 0:1‘ an an‘ E all‘ 0 s. b I. 3 bI 3 bl‘ b bII bm bII’ B I /3 I‘ K3 /3 I,


/3 II‘ /3 II p 11* Egg mst { m st. Mst mesoderm zmlage luau’ ,L-L stomodeum anlage (TT EMSt I EI ° 51 E primitive endoderm EII ° " \ 8 II P‘ cl C {en C ectomesoderm yl y { yII P, d D {5 secondary mesoderm P: { G . P4 _ germ line (:1

CELL LINEAGE OF ASCAEIS FROM DESCRIPTIONS OF ZUR HTRASSEN AND BOVERI

line continues for five cell generations, at the end of which time no further somatic cells are produced from this line and the cells rest from further division until the organism has reached a considerable degree of maturity. The distinction which is made possible by following through the chromatin diminution between germ plasm and soma in these early blastomeres of Ascaris has been of great theoretical significance and often referred to as evidence in support of the theory of germinal continuity. In this connection it is further discussed in Part Two, Chapter I. The process will be more clearly understood by referring to that discussion and also to the table showing the cleavage of Ascaris which appears herewith.

5. Rotifers

The remaining example of the bilateral type of cleavage is that of the rotifers. This example is not in many respects characteristic of the type and its development is not fully understood. It is to a certain extent intermediate between the bilateral and the spiral types. The retifers have no cleavage cavity or gastrula cavity. (That is, they have stereoblastulae and stereogastrulae.) The resemblance between the developmental conditions of annelids and rnolluscs and of the rotifers is perhaps not so surprising in view of the fact that all these groups pass through larval stages which are_ morphologically trochophores.

Although the character of the cleavage of rotifers is sufiieiently bilateral to be placed with other forms of this type, the peculiarities are such that it seems unnecessary to follow out the details for these forms.

IV. SPIRAL CLEAVAGE

Spiral cleavage is characteristic of polyelads, nemerteans, polychaetes and many molluscs. Eggs which cleave spirally are with few exceptions well filled with yolk and therefore segment unequally. Frequently the inequality is so great that only a small cap of cells comprising the ectoderm lies on the large endodermal cells with a consequent more or less complete reduction of the cleavage cavity. This condition also results in a much modified type of gastrulation from that which is characteristic of holoblastic eggs.

Nevertheless it is not difficult to derive the spiral type of cleavage from the equal radial type. The first two cleavages are meridional and about at right angles to each other, thus dividing the egg into four nearly equal blastomeres. In the 4-cell stage blastomeres A and C (see nomenclature below) are nearer the animal pole than B and D and form with each other what is known as a polar furrow, as do B and D at the vegetal pole. But the polar furrows at the two poles are perpendicular to each other. The departure from the radial type becomes clearly distinguished in the third cleavage, owing to an oblique shift in spindle direction so that when viewed from the animal pole the upper end of the spindle is turned either to the right (which is the usual ease) or to the left. Bearing in mind the fact that the yolk is massed at the vegetal end of each blastomerc and the pure cytoplasm at the other ends, and the general rule (Sachs-Hertwig laws) that a spindle axis tends to lie in the center of the cytoplasmic mass, one sees that an unequal cleavage of each of the four blastomeres will occur. They are divided into small upper cells or micromeres, and large ones in the lower hemisphere or macromeres, and the upper quartette of cells thus arising alternates in


fiG. 27. (‘nmp:mLti\'o diugrzuns of radial and spiral cle:tvn.ge. (Redrawn from Korsehelt and Helder.)

A, mdinl type; B, spiral type in third cleavage; C, D, rudial and the spiral type respectively in fourth cleavage.

position with the lower (fig. 30 c, e). The upper quartette of cells, called ectomeres, appears to be given off spirally from the lower endomeres, although of course speaking strictly it is not correct to think of these cells in this manner, for both quartettes are composed merely of the daughter cells of the preceding 4-cell stage. This third cleavage is said to be a dexiotropic or right-handed division since the cells of the ectomere quartette are turned 45 degrees from those of the macromeres in a right spiral.

The fourth cleavage ‘spindles are now formed in accordance with the general tendency expressed by the so-called alternation rule that successive cleavage planes tend to intersect each other at right angles. The spindles, therefore, take up such positions that the next divisions are laco

fiG. 28. (‘ontinuutinn of fig. 27. Polar views.

A, 13. 8- and 113-0011 stages rarlinl type; (3, I), third and fourth cleavages, spiral typo; E. 1". 8- and 16-cell stages spiral typo.

tropic, that is in the direction of left-handed spirals. This alternation continues in regular order until four quartettes have been produced, and meanwhile each of the cells divides according to the same general laws of E

fiG. 29. Cleavage of Crcpzdula. (Redrawn from (‘onklin.)

A. resting stage after the first cleavage; blastomeres flattening against each other and nuclei. asters, and protoplasmic area rotated dexiotropically; B, anaphase of the second cleavage. The shift which will result in the formation of a polar furrow just beneath the polar bodies is already making its appearance, C‘, completion of the second cleavage Polar furrow well formed; D. third r-leavage; E, side view of egg in 29-cell stage. The relation of the mesontoblast coll 4d is shown to the macromere D.


cleavage. Since the blastomeres of spirally cleaving eggs are always unequal, differences occurring even within a quartette as well as between different quartettes, it follows that the cleavages cannot long remain entirely regular, for differentiation is rapidly taking place.


Owing to the fact that spiral cleavage is one of the most markedly determinative in character, this form presents an unusually good example for the study of cell lineage. To bring out the relationships between cells it is found to be necessary to have a definite terminology and nomenclature for the blastomeres of eggs of this type. The system adopted by Conklin for expressing the relationships in the case of Crepidula is now in general use. Certain special cells should be given special names, but in general the system adopted should show immediately the derivation of each cell by its name. For this purpose Conklin modified the system previously introduced by Wilson to describe the cell lineage of Nereis.


In the nomenclature used in Crepidula Conklin designated the quartettes of cells by coefficients: “e.g., the first quartette of micromeres and all their derivatives are designated by the coefficient 1 (la, ld, la‘-2, 1c”, etc.), the second quartette and its progeny by the coefficient 2 (2a, 2d, 2c3-1, etc.), the third quartette by the coefficient 3 (3a, 3d, etc.), and the fourth quartette by 4 (4a, 4d, etc.).” It is desirable to emphasize in this manner “the differences between the quartcttes of micromeres because in general their histories are very different,” and because the distinctions afford the basis for tracing the cell lineage in the more advanced stages. The coefficients designating the quartettes are retained in all subsequent stages and the further cell lineage indicated by exponents. The cell la divides to form la‘ and la“. Then further exponents are added for each new cell generation always retaining the complete designation of the parent cell. The cell la“ produces la?‘ and la”; la“ produces la?“ and 1am, etc. These are the designations used for the micromeres and their descendants.


The second division resulted in the formation of four blastomeres, A, B, C, and D. (Capital letters are used to indicate macromeres.) These divided in turn to produce 1A and la in the A quadrant of the egg and similarly in the other quadrants. Each successive macromere receives a new coeflicient as it divides into a new macromere and a micromere; thus 1A produces 2A and 2a; 2A in turn 3A and 3a. Numerical coefficients are used to designate successive quartettes, while the exponents indicate the products of their division. Cleavage is dexiotropic, or oblique to the right, if the spindle direction is turned clockwise from the axis of the egg, and laeotropic when turned to the left.

By reference to the accompanying table the relationships of the blastofiG. 30. first cleavage of Crezridula plana. (After Conklin.)

A, approach of sperm and egg pronuclei; B, nuclei in contact, asters and centrosomcs at their pole, central spindle not yet formed; C, central spindle appearing between the two cleavage centrosomes; chromosomes aggregating on the spindle; other granules dis— solving. Sphere substance increased in size and radiating into the cytoplasm; D, prophase of the first cleavage. Chromatin granules assuming their relation to the spindle fibers; E, metaphase of the first cleavage; F, telophase of the first cleavage; spindle axis bending. Nuclei of left cell partially divided indicating origin of upper part from egg pronucleus from female and lower from-the male.

meres and their fate will be more clearly understood and the application of the system of nomenclature shown for this case.


In general the 8-cell stage of an egg with spiral cleavage consists of four micromeres, 1a, 1b, 1c, 1d about the animal pole, and four macromeres, 1A, 1B, 1C, ID, at the vegetative pole. In most cases the third cleavage is dexiotropic. The 16-cell stage is reached by a aeotropic division and consists of the quartettes of micromeres, la‘,1b‘,lc’,1d‘, 1a’,1b’,1c2,1d?, 2a,2b,2c,2d,andonequartetteof1nacr0meres,2A ,2B,2(,‘, 2D. There is an intermediate condition in eggs having spiral cleavage in which there are actually twelve cells only, for the second quartette, 2a to 2d, is budded off before the division of the first, 1a to 1d, is completed. There is a similar lack of regularity of division in other stages, some quartettes dividing while others hold back even to the extent that some cells may be an entire cell generation behind others. In the transl A B Fm. 31. Cleavage of Trochus. (Redmwn from Korsehelt and Heider, after Robert.) A, 8-cell stage viewed from the side (the D quadrant will become the dorsal side); similar view of 16-cell stage. tion to the 32-cell stage there is actually no resting stage in the sense that all the cells are at once in that same state of progress.

The division producing the 32-cell stage is usually a dexiotropic one. The cells of the first quartette receive their second exponent, la‘ becoming la" and la”; those of the second quartette their first, 2a‘ and 2a’; and the four macromeres divide, producing 3A and 3a (using the A quadrant as a sample). There are now sixteen descendants of the first quartette and eight of the second.


The 32-cell stage brings to the spiral type of cleavage a certain degree of completeness, for three successive divisions have produced three quartettes of ectomeres that represent chiefly ectoderm-forming cells, although larval mesenehyme is also produced from some of the derivatives of the second quartette. The four macromeres subsequently produce two more quartettes of micromeres and are in general endodermforming cells. An exception is found in the cell 4d in the higher forms having spiral cleavage, for it is the parent cell of the mesoderm. SPIRAL CLEAVAGE 57


In later stages some blastomeres are found to divide meridionally, and the necessity appears of a new criterion for numbering the products. In such a case the dcxtral cell is given the exponent 1 and the sinistral 2. The succession of alternating left and right divisions continues to the 64-cell stage. Later on bilateral conditions develop and the embryo takes on the symmetry of the adult.


Spiral cleavage, as already indicated, occurs in several of the great divisions of the animal kingdom. It first appears in the polyclads. Our knowledge of the cleavage of this group is based especially upon the study of Discocoelis by Lang, of Leploplana by Wilson and of Pltmocera by Surface. Cleavage in these forms follows the general scheme as previously given for all of its main features. There are variations due to differences in the size of the blastomeres and other such factors, but the general plan as described is entirely applicable here. There are certain features in the development of these forms which suggest a relationship to the cleavage of the other flatworms, but there are a great many points of agreement between the method of cleavage of polyclads on one side and that of the annelids and inolluscs on the other, and it has been held by the most careful investigators that a true homology exists with respect to the early development of these forms. The points on which the agreement is observed are sufficiently important that they seem to indicate more than a mere adaptive coincidence on the part of the previous types of the two groups. The formation of three ectomere quartettes which alternate in dexiotropic and laeotropic formations, the agreement in the relationships of the cells of the quartette 1a2—1d2 with the primary trochoblasts of the annelids and molluscs, and complete homology in the development of the mesoderm and also in the formation of the ectodermal structures near the animal pole, all seem important in bringing the polyclads into line with the annelids and molluscs.


Fig. 3'2. of ('4-rt-bralrz/u~c marginalus. (Redrawn from Korschelt, and Heider, after Zeleny.)

.\. R-cell stage; B. 16-r-ell stage; (‘, :.’.2s’»cell stage from side view; D. 28-cell stage from \'egetati\"e pole.



The nemerteans also conform to the general method of spiral cleavage, and indeed they are almost diagrammatic in the regularity which they show. The studies of Coe on Micrura, of C. B. Wilson on Cerebratulus lacteus, and of Zeleny on Cerebratulus marginalis are sufficient to establish the important features of cleavage in this type. The work on these forms as well as upon others of this group is so similar to that described for other cases that it does not seem necessary to consider it in detail although it is important and of excellent character.


Spiral cleavage is especially developed among the polychaetous annelids. Of special importance are the studies of E. B. Wilson on Nerezls-, of Child on Arenicola, as well as the observations of Mead, Treadwell, Nelson, Torrey, and Gerould on other forms of polychaetes. The later stages have been made more clear by the work of Woltcreck on Polygordius. The cleavage of Arenicola, which leads to the development of the trochophore larvae in its fundamental features, corresponds to that of the general type already described. The cleavage axis running from animal to vegetative pole corresponds to the chief axis of the troehophore larva, and although the first cleavages present slight differences in order and in the angles they make with the egg axis the result is the same as in the general type, for by the time of the 8- and 16-cell stages the normal relationships have been returned although there are certain marks of size differentiation among the various blastomeres. The differences which exist between the cell lineage of Arenicola and that of the type form are minor differences only. There are, however, some special features about the cleavage of the annelids which deserve mention. In the animal half of the egg there presently develop certain configurations which are especially useful in homologizing the blastomeres of these forms with those of the very similarly cleaving eggs of the gastropod molluscs. The blastomeres about the animal pole arrange themselves to form what is known as the cross of the annelids, and this becomes the chief characteristic of the embryo for the stages immediately following the 64-091] condition. As will be seen by consulting the accompanying fiG 33 ('le.nu.go stage of Anmcula cnstata (RC-drawn from Korichelt and Helder, after (‘hxld )


A, 1)-coll stage, B, 4-coll stage C, “Hell stage I), 16-coll stage Pnmary trochoblasts are stxppled, E, the apu-nl stun culls la"-Id“ are dwldmg to produce m F the apical rosette cells 19.1”-ld'“ and the stem cells of the cross 1a“‘-Id“? The primary trochoblasts are la"-Id" and 121 figure there are in each quadrant apical rosette cells, stem cells of the cross and intermediate cells. These cells when the four quadrants are considered together form a very definite picture of a cross, and not only are the cells themselves homologous with the similar condition found in the gastropods but there is a decided similarity in their arrangement, as will be seen by comparing fig. 33 for Arenicola with the similar figure of Crepidula (fig. 29).


The first appearance of the mesoderm in Arenicola is from the cell 4d which has come to be known as cell 111. Here again the homology between the annelid and gastropod types is quite complete. The study of cell lineage in the annelids was carried on so thoroughly and the results were so beautifully worked out that there are many other features in the development of this group that call forth the admiration of the observer to the precision of the developmental mechanism. This is determinative cleavage at its best and the specialist in this field of embryology finds a great deal here to interest him.


The cleavage of the Oligochaeta and the Hirudinca with certain modifications shows the general agreement with the type just discussed. These differences are correlated with the differences in the mode of existence between the water-living polychaetes and the other more specialized classes of annelids. In one of these forms, Clepsine, a leech, the first study of cell lineage was made by Whitman in 1878.


As already indicated, the most important studies of the spiral type of cleavage have been made in various molluscan eggs. Here there is a wealth of observation and the literature contains many excellent accounts of the cell lineage of these forms. Only a very few can be mentioned including the following. For the Amphineura there are the observations of Metcalf on ('hz'ton and Heath on I schnochiton; for the Lamellibranchia those of Lillie on U me. The gastropod eggs have been especially studied as is indicated by the following investigations on the three subdivisions of this class. Conklin on Crepidula, Robert on Trochus are especially important contributions to our knowledge of the development of the Prosobranchia, as is the work of Heymons on Umbrella, Casteel on fiona for the Opisthobranchia, and Holmes on Planorbis and Wierzejski on Physa for the Pulmonata. Many other forms have been studied, but these are examples of the various conditions found here. It may be noted that the cleavage of Planorbis and of Physa may be readily followed in the laboratory, at least during very early stages, and they present perhaps the best opportunities for a student to observe this type of development.


Spiral cleavage in the molluscs conforms to the type and indeed might serve as the type, as may be seen from the table summarizing the development of Crepidula. The importance of the homologies existing between the blastomeres of the annelids and of the molluscs have already been pointed out and need not again be referred to. Certain other interesting features, however, should be noted. One of these is the presence of the yolk lobe described by a number of investigators in heavily yolk-laden Inollusc eggs. A similar structure has been described also in some annelids. Here there appears at the vegetative pole in each of the first few cleavages a lobe Inore or less clearly marked but never completely cut off from one of the blastomercs. It is known as the yolk lobe and is of varying size in different animals. Before each succeeding cleavage it unites again with its blastomere, only to present itself in the interim before the next cleavage. finally it becomes completely united with the cell D and development proceeds. Experiments have been performed in which this lobe has been cut off with the result that the larvae lack the ectoderm of the posterior portion of the body. Another interesting phenomenon observed in some cases of spiral cleavage concerns the relation between the symmetry of the adult and that of the embryo. Crampton pointed out as a result of studying the cleavage of Physa that the reversed spiral of the shell of this snail is not a matter of adult life only but is so definitely impressed upon the nature of the species that the direction of the cleavage planes from the third division 011 is exactly reversed from what is seen in eggs in which there is a shell coiled in a right-handed spiral.


The later stages in the cell lineage of spirally cleaving eggs lead us to a consideration of the methods of gastrulation and of mesoderm formation and as such seem more properly to be considered in the chaptels which deal with these matters.

Bibliographic Note

Among the more important accounts of the subjects contained in this chapter are the following: Echinoderms: Korsehelt and Heider, Selenka, Boveri, Plough, Morgan (Experimental Embryology); Ctenophores: Ziegler, Metchnikoff; Amphioxus: Cerfontaine, Hatschek; Ascidians: Conklin, Chabry, Castle, Drieseh; Frog: Brachet, Morgan; Ascaris: Boveri; Spiral types: Conklin, Holmes, Wilson, Child, Lillie, Robert, Coe, Lang, Surface, Whitman, Metealf, Casteel, Wierzejski, Crampton. These works are cited in full in the bibliography on page 406.


1931 Richards: Part One General Embryology 1 Historical Development of Embryology | 2 The Germ-Cell Cycle | 3 Egg and Cleavage Types | 4 Holoblastic Types of Cleavage | 5 Meroblastic Types of Cleavage | 6 Types of Blastulae | 7 Endoderm Formation | 8 Mesoderm Formation | 9 Types of Invertebrate Larvae | 10 Formation of the Mammalian Embryo | 11 Egg and Embryonic Membranes | Part Two Embryological Problems 1 The Origin And Development Of Germ Cells | 2 Germ-Layer Theory | 3 The Recapitulation Theory | 4 Asexual Reproduction | 5 Parthenogenesis | 6 Paedogenesis And Neoteny | 7 Polyembryony | 8 The Determination Problem | 9 Ecological Control Of Invertebrate Larval Types


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