Book - Outline of Comparative Embryology 1-5

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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 V Meroblastic Types of Cleavage

I . Superficial Cleavage

Superficial cleavage is found to occur most extensively among the arthropod classes and indeed by many it is supposed to be coextensive with this phylum of animals. There are, however, some other cases which may be properly spoken of as superficial cleavage. Among these latter are the eggs of some eoelenterates which are heavily laden with yolk, for example, Renilla, hydrocorals and Alcyonium. In addition it has been described for the holothurean, Cucumaria glacialis.

Furthermore, it is by no means true that all arthropods undergo superficial cleavage. Among the Crustacea there are many cases of total cleavage in holoblastic eggs, and at the other extreme of the phylum the scorpions have discoidal cleavage. Examples of holoblastic cleavage may be chosen from Branchipus (Brauer, 1892), Artemia, Lucifer, some parasitic copepods, the cirripeds and most frec—living copcpods. These examples include cases in which cleavage is very nearly equal and in others, as the cirripeds, distinctly unequal. One illuminating study has been made on the cleavage of the barnacle Lepas, which suggests relationship to the annelid type and even has certain characteristics of the rotifers. In view of the generally assumed fact that the arthropods are derived from annelid ancestry, the case of Lepas as studied by Bigelow seems to have unusual importance.

With the exceptions of the forms mentioned the arthropods have superficial cleavage. It will be observed that the diversity of this phylum is so great that many different conditions of cleavage are found here and even among the cases of superficial cleavage there will be seen to be a great variety. To such an extent is this true that we cannot describe as typical of superficially cleaving eggs any one particular form, and, although we may classify superficial cleavage into subdivisions, these are by no means separated from each other sharply but gradations exist between them. Superficial cleavage is characteristic of eggs which are centrolecithal in character; eggs of the centrolecithal type are derived from forms having total and in most cases equal cleavage, while on the other hand they lead to an extreme type of superficial cleavage which is so different from the usual arthropod eg as to be classified with eggs having discoidal cleavage rather than superficial. Reference is made to the eggs of the scorpion which are without question derived from the extreme superficial type but which as a result of parallel convergence resemble most clearly the discoidal type of vertebrates. In eentrolecithal eggs the cleavage nucleus is usually at the center of the egg and is surrounded by the mass of yolk spherules and fat droplets. Penetrating this mass in every part is a network of cytoplasm which is continuous with the central cytoplasmic portion around the nucleus and also with a very thin superficial cytoplasmic layer on the outside of the egg. This latter layer is in some cases so delicate as to be difficult to make out, whereas in other cases it is clearly visible. It is to be regarded as characteristic of the centrolecithal egg, however. The shape of these eggs varies from spherical or elliptical to a greatly elongated, almost cylindrical type, but they are seldom “egg shaped” in the sense that they have one blunt and one pointed end. There is practically no trace of an axial structure which is characteristic of so many other egg types.

As a first type of superficial cleavage we may take up one of the insects, for in this form it is especially clearly developed. The well-known figures of the cleavage of Hydrophilus suggest the early course of this type of development. The cleavage nucleus lying at the center of the egg in the midst of its plasma island divides into 2, 4, 8. 16 nuclei, each surrounded by a small portion of cytoplasm and each somewhat separated from the others in the form of amoeboid or star-shaped areas. Actually all are in communication through the plasma. network that penetrates the yolk mass. At this stage and for some time later the egg actually is a syncytiuln, for there are no definite cell boundaries marked off around any nucleated areas. It has been the practice on the part of some writers to speak of these areas as cleavage cells, although they are not cells in the sense of other types of cleaving eggs. After a few divisions these cleavage cells come to form a layer within the yolk which by one continued division tends to approach the periphery of the egg. At length they unite with the superficial cytoplasmic layer in Hg/drophilus near the middle of the egg first and at the ends only some time later. Then cytoplasmic boundaries become visible and the cleavage is truly superficial, although of course only partial, since the divisions do not extend through the yolk mass.

In insect eggs it frequently occurs that some of the cleavage cells do not take part in the formation of the blastoderm but remain in the yolk while the others pass to the surface. They take on special functions for the assimilation of the yolk substance and become known as the mellophages. In some cases incomplete cell boundaries seem to be formed fiG. 34. Blasboderm formation in the water beetle Hydrophilus. (Redruwn from Korschelt and Heidcr. after Heider.)

b, blastoderm cells; 0, “cleavage cells"; p, peripheral layer of protoplasm; y, yolk.


around these vitellophages, giving rise to the so-called secondary yolk cleavage. The vitellophages are to be regarded as endoderm, and for that reason some investigators have described superficial cleavage as leading directly to the formation of a gastrula-like stage since two kinds of cells, ectoderm and endoderm, are formed about the same time. This view has not been widely adopted.

Superficial cleavage usually results in the formation of blastomeres of equal size and cleavage is indcterminativc.* Inequalities appear very early in some forms, however, and there are many variations from the forms of the cleavage as already given for Ilytlrophilus. These variations seem at first sight to correspond in a general fashion to the systematic groups of the arthropods, for the crustacean eggs are distinguishable from the spiders and from tl1e insects, by certain characteristic features; but these differences do not lend themselves to accuracy of statement nor form a satisfactory basis for classification. It is wiser therefore to classify the superficial cleavage under the following heads: Group 1. Cleavage at first total but later superficial. Group 2. Cleavage purely superficial. Both of these groups in their turn may be divided into two subdivisions in one of which the blastoderm forms on all sides simultaneously and in the other on the ventral side precociously.

1. Cleavage at first Total but Later Superficial

This type of cleavage, which is typical of many crustaceans, begins with the division of the plasma island into 2, 4, and perhaps 8 blastemcres about which all cell boundaries are cut off at once. (‘leavage during this period of the development and for some successive cell divisions thereafter is total and approximately equal. Presently there comes a time when the furrows at the surface are unable to cut entirely through the egg, or if they do the yolk masses at the center must fuse together and cleavage becomes superficial with a cellular region sharply separated from the yolk mass. The blastula consists of a layer of superficial cells of cq11al size and an inner yolk mass replacing the cleavage cavity. In many cases there is a (listinction between the central-lying yolk mass and the yolk which formed the inner end of the blastomcre. They were left incomplete by the failure of the furrows to penetrate to the center of the egg. These inner ends are spoken of as the yolk pyramids (sometimes as Rathke’s yolk pyramids). The significance of these structures is not entirely clear but their appearance is characteristic. This type of cleavage easily suggests a transition from the holoblastic eggs of other Crustacea to the form in which cleavage is purely super. ficial. This type of cleavage, as already pointed out, occurs in two subdivisions :

Nevertheless, experiments on the egg of the house fly, M usca domestica, made by Reith (1925) show for this animal (and make it probable for others having this type of cleavage) that the egg is highly determinative. The embryo is fore-shadowed in the cytoplasm of the egg and the regions are clearly organized in relation to their future destiny. Add to this.the very definite nuclear determination which the experiments on the genetics of Drosophila have demonstrated, and it is clear that the eggs of Dipteru can by no means he called indeterminative.


fiG. 35. Cleavage of Macrutoma vulgaris. (Redmwn from Korsehelt and Heider, after Uzel.)

A, two cleavage nuclei; B, four cleavage nuclei; C, section through 16-cell stage with blastomeres completely separated from one another; D, similar section through 32-cell stage. E, F, later stages in the formation of the blastoderm. the yolk mass in the center having fused.

a. Eggs in which the superficial cleavage leads to blastoderni formation simultaneously all over the egg. To this subdivision belong the eggs of those free-living copepods which are not holoblastic, some parasitic copepods, the ostraeods, spiders, and some isolated forms in various groups of the arthropods.

b. Eggs in which the blastoderm develops early on the ventral side, a condition which foretells the position of the forming germ streak. The dccapods in part come under this subdivision as do some of the amphipods as well as other scattering forms.

2. Eggs with Purely Superficial Cleavage

Eggs which come under this subdivision carry still farther those tendencies which are beginning to be expressed in the previous group.

fiG. 36. Cleavage of the crab Dromfa. (Redrawn from Korschelt and Heider. after Cane.) Successive stages showing “cleavage cells," the yolk pyramids, and the blastoderm.


The cytoplasmic portion of the egg is quite unable to control the yolk mass and therefore the cleavage cannot be complete. The central-lying nucleus with its surrounding plasmic layer divides several times but no cell boundaries are formed by the separate areas. The only indication of division now to be seen is the occasional presence of superficial furrows which do not penetrate far into the yolk. As the cleavage nuclei increase they approach the surface and furrows become more pronounced. The result is a blastoderm with the cell boundaries cutting in to the yolk although not completely delimiting definite cell bodies from it until a. later stage when the blastoderm takes on the form of the definite layer. Cleavage of this type occurs among the Crustacea commonly, although it is much more widespread in the Malacostraca than in the Entomostraca. In some of the latter, however, this condition has been described. In the Malacostraca it is the most common form, occurring in the Decapoda (with the exception of those previously mentioned), Nebalia, Cumaceae, the Schizopoda, and Isopoda. It is found also in some of the mites, in nearly all insects, in the Myriapoda and in the ()nychophora. With a distribution so widespread as this it is obvious that many variations will be found, although in general the description of Ilyrlrophilus as already given is quite applicable. There are cases in which the superficial plasma layer is so thin as to be almost absent and other cases in which it is Very definitely marked and these varying conditions have an effect upon the appearance of the blastoderm. There is also variation in the extent to which the blastoderm is formed over the surface of the egg. This latter feature is the basis for the further classification of these eggs into two types as in the previous group.

1. Eggs which have simultaneous formations of the blastoderm all over the egg. Most of the cases of purely superficial cleavage come here, specifically the Cladocera, most decapods, the myriapods, most insects and many other scattered forms.


b. Eggs with precocious development of the blastoderm on the ventral side. Here belong Ncbalia, the schizopods, the Cumaceae, the isopods, and some decapods,including the lobster. The restriction of the blastederm to a small portion of the surface of the egg is so marked in some of these forms that it was formerly the practice of some investigators to regard these as cases of diseoidal cleavage. We do not at the present time, however, so regard them. Nevertheless this subdivision of superficial cleavage clearly leads to the conditions found in the scorpions as an extreme case, and these latter forms are commonly included with the cephalopods and meroblastie vertebrates under the head of discoidal cleavage.

II. DISCOIDAL CLEAVAGE

Discoidal cleavage is the type generally found among the meroblastic vertebrates, and it occurs also in the ascidian group, the pyrosomes, and in two separate invertebrate classes, the cephalopods and the scorpions. This distribution suggests what is found to be the case, namely that fiG. 37. Cleavage of (”am7mdz'a staphulinus. (Rcdrawn from Korschelt and Heider, after Uzel.)

Sections showing cleavage and formation of the blastoderm. In F the thickening on the ventral side which will give rise to the blastoderm is to be noted.

discoidal cleavage is derived from simpler, unlike, and unrelated cleavage forms. It may be assumed that the vertebrate type is derived from an extreme case of telolecithal egg in which there is sufficient yolk present to prevent the cleavage furrows from cutting entirely through the egg. This results ‘in a certain degree of opposition between the animal or protoplasmic portion of the egg as contrasted with the vegetative or yolk region. Similar relationships obtain for the other groups having discoidal cleavage except the scorpions in which the discoidal type is derived, as may be inferred from the preceding discussion (page 68) from the extreme case of purely superficial cleavage. Only a small portion of the egg surface is involved in the formation of the embryo body in the superficial forms mentioned.

It is evident that not much in common is to be expected in the elemental features of these two characteristic modes of discoidal cleavage.


fiG. 38. Germ disc of the scorpion Euscorpius carpathicus. Polar views. (Redrawn from Korschelt and Heider, after Brauer.)

It was formerly said that discoidal cleavage occurs also in some crustaceans but it seems wiser to regard these as within the limits of superficial cleavage than as examples of the true discoidal type. Because of the separate origin of these cleavage types it will be convenient to begin this discussion with the cleavage of the scorpion.

1. Scorpions

Only one important piece of investigation, namely the study of the cleavage of Euscorpius, by Brauer, is available upon which to base our knowledge of this type. The egg is richly yolk laden and the protoplasmic portion is limited to a disc-shaped area which corresponds to the point of attachment within the egg follicle. With the exception of perhaps a very thin filament over the surface of the egg no other protoplasmic portion can be demonstrated. Segmentation is limited to the protoplasmic disc which divides with fair regularity. About the third or fourth cleavage there is oftentimes what seems superficially to be a bilateral arrangement of the blastomeres, but the appearance is only superficial for the cleavages from here on become quite irregular result of cleavage is a round or oval blastodisc consisting of at first but a single layer of cells. The single-celled condition does not remain long because a number of cells wander down below the surface from a definitely recognizable white speck. This speck is important in determining the plane of symmetry and the hinder end of the embryo. The first cells which wander in are transformed into yolk cells and although they form an irregular layer they take no further part in the development of the embryo. Very shortly after the migration of the yolk cells a group of cells becomes differentiated as a result of ingrowth from the same region and is said to give rise to all the genital cells. True endoderm cells also appear in like manner at the same time. Brauer holds that the endoderin cells do not contribute to the formation of yolk cells nor do the yolk cells take part in the formation of the endoderm.


Fig. '3‘) Set tions of stages similar to lig .58, and of two liter stages.

A, immature germinal vesicle, B, early cleavage, C‘, l)l‘1‘lt()(l(‘l‘II1 formed, D, beginning of germ layer forniition showing segregation of the germ cell g < and of the endodi-rm, en E, later stage in germ layer form then cc cctoderm, mes mesoderin, so serosa



Mesoderm arises from a division of cctoderm cells near those which are to produce genital cells. The subsequent development of the blastedisc shows the formation of a segmented germ streak which gradually develops into the typical body form of the scorpion and which grows finally to include entirely the yolk in the middle region of the gut. The forming embryo is suggestive of certain stages in the later development of eggs having superficial cleavage but it is likewise very similar in a number of particulars to the conditions found in vertebrate embryos which develop by diseoidal clcivage. There are clearly produced in these different groups similarities which are purely embryonic and therefore transitory; they have no evolutionary significance.

2. Cephalopods

The cleavage of cephalopod eggs differs in many particulars from that of other molluscs and also from the forms within the groups having discoidal cleavage. The differences seem to be in keeping with the peculiarities of egg structure, which are pronounced.


The eggs are laid in large numbers, usually together, and the mass may assume various forms. There is always a protective covering which is the means of attaching the mass of spawn. In Sepia the eggs are discrete and each is in its own capsule. In Loligo many are laid together in a gelatinous tube and numerous tubes are attached in one mass, known to the sailors as “dead men’s fingers.” Fertilization follows after various peculiar types of copulation in which spermatozoa are transferrerl in spermatophores; fertilization is internal in some groups, and external in others, of which the squids mentioned are examples.



Fig. 40. Eggs of the squid Loligo pmlii. (Redmwn from Korsehelt and Heider, after Watase.) d. dorsal, v. ventral, a. anterior, p. posterior, r. right, I. left.


The eggs themselves are relatively large for marine eggs and all contain very much yolk. The development of the squids, particularly of Sepia and of Loligo, are best known and will be used from here on as examples of this form of development. Sepia eggs have the size of ordinary peas, whereas those of Loligo are much smaller, but even they are larger than the eggs of most marine molluscs.


Cephalopod eggs have been studied by numerous investigators, but our knowledge of the cleavage depends chiefly upon the work of Vialleton on Sepia ofiicinalis and of Watase on Loligo pealii. The eggs of Loligo, at the time they are ready for cleavage, are somewhat oblong in shape, one end being more pointed than the ot.her. The egg consists of a mass of fine granules of food yolk surrounded entirely by a thin protoplasmic layer. This layer is thicker at the pointed end of the egg where the germ disc will form. Thus this egg represents an extreme telolecithal type and is a perfect example of meroblastic cleavage.

The uncleaved egg from surface study alone gives evidence of bilateral symmetry which bears a definite relation to the subsequent history of the embryo, and it is possible to distinguish an anterior border from a posterior as well as right from left sides of the organism. The germ disc end of the egg corresponds to the dorsal side of the embryo and the


fiG. 41. Germ disc of the squid Sepia 0j7'i(‘inaIi.~r. (Redrawn from Korsehelt and Heider, after Vialleton.)

I to III, indicates direction of su('r'essive cleavage planes.

yolk pole to the ventral side. On the anterior side the germ disc extends farther down toward the equator than upon the opposite side, but it is symmetrical with respect to right and left. The animal pole of the egg is slightly eccentric to the center of the germ disc, being nearer its posterior edge. Here in Loligo may be seen three polar bodies in the perivitelline fold inside the chorion. The egg is surrounded by chorion which is secreted by the follicular epithelium and is often very tough. The sperm enters through a mieropyle in this chorion.

The early cleavages are limited to the germ disc. The first furrow corresponds to the median plane of the future embryo, dividing the egg into right and left halves. In the center of the blastodisc it cuts in deeply, dividing the entire protoplasmic cap at this point, but toward the edges of the disc it becomes shallower until it is a mere groove and finally disappears entirely. The successive cleavages behave in a similar manner. Thus cleavage is incomplete even with respect to the protoplasmic layer. ,The second furrow is at right angles to the first, and like it, fades away into the thin protoplasm. The later furrows which extend outward likewise fade away and the cells thus formed are incompletely separated peripherally. This gives rise to the distinction made by Vialleton of the products of cleavage into blastomeres and blastocones,



Fm 42 Older germ disc of S(’[)’LLl ofiicmalzs from the beginning of germ layer form itu n The darker cells iiidimte the region where the disc is of several cells in llll( kiiess L itcr stage than fig 41

the term blastomere being applied only to those cells which are conipletely cut off, while the peripheral ones which have no outer boundary are spoken of as blastocones.

In the preceding types of cleavage we have seen that the cleavage cells have usually received special designations. In the present case, on the other hand, it has been found more convenient to indicate a distinction between the various cleavage cells by numbering the furrows which separate them, the first furrow lying in the median plane and indicated by the polar body numbered I. The second furrow, II, is at right angles to it. The third furrow likewise is meridional but it divides the two anterior blastomeres and blastocones equally and runs obliquely to the previous furrows. The two hinder blastocones are divided very unequally, for furrow III is almost parallel to the median plane and cuts off two very narrow segments. In the fourth division the inner ends of these narrow segments are cut off to form the first two blastomeres by the transverse plane. The remaining six cells are again divided in a direction which is correctly spoken of as meridional, although the various planes are not entirely regular and do not converge at the center of the disc. By this time the bilaterality which existed in the uneleaved egg has become very appaient, each half of the egg consisting of seven blastocones and one blastomere. The 32-cell stage is reached partly by nieiidional and partly by transverse furrows. Numbering the blastocones of each half of the egg from the anterior side backwards as one to six, the following divisions occur. Number one divides transversally, producing a blastoinere and a blastocone. Numbers two and three divide meridionally, each producing two blastocones. Numbers four and five each cut off a blastomere by a transverse division, and number six divides meridionally. The posterior narrow pair of blastocones again divide transversally, cutting off blastomeres, and the two first blastemeres likewise divide. The 32-cell stage thus consists of fourteen blastemeres and eighteen blastocones symmetrically arranged. Thus the center of the disc comes to be filled up with a compact layer of blastomeres radiating from ‘which are the blastocones.


fit. 4i Se: tioim ilirmigh the edge of the germ (.lls( in suctessiic stagm B, corresponds to fig 42 y, yolk, y 0 , yolk epithelium, e, embryonic cells



Subsequent cleavages bring about a decrease in the size of the blastemeres and are responsible for their regular disposition. The germ disc thus comes to consist of a one—layered plate of polygonal cells with peripheral blastocones passing over into the mass of formative yolk. Gradually these peripheral cells detach themselves from the germ disc and scatter about the surface of the food yolk. It is claimed that they even wander beneath the cells of the germ disc and gradually form a layer which spreads over the entire yolk. The solid blastodisc at length becomes many-layered and by its extension grows over the layer of yolk cells derived from the blastocones.


The relationship of the primary germ layers of the cephalopods is complicated, and the manner in which the embryo body is formed is not properly a subject for detailed discussion here. The reader is referred to the descriptions of these processes in more extensive works.

3. Vertebrates

The most characteristic and best-known cases of discoidal cleavage occur among the chordates. There is a single example among the lower chordates, that of the pyrosomes, which has some resemblance to the discoidal type as found in teleost eggs. In pyrosome eggs, however, certain cells around the edge of the disc recall the blastoconcs of the cephalopods.


Among the vertebrates proper discoidal cleavage occurs widely in scattered groups. It is found in the myxinoids, the elasmobranehs, teleosts, Gymnophiona, all reptiles and birds, in the inonotremes, and it has been recorded for some Inarsupial eggs. In the opossum, however, according to the accurate and clear description of Hartman, cleavage is certainly not disceidal, nor is that of Dasyurus as figured by Hill. Thus it occurs in five classes of vertebrates, and possibly in the sixth; in seine of these it is the characteristic method and in others it is quite exceptional. This distribution points out, as has been noted previously, that there is no taxonomic or phylogenetic significance in the classification of cleavage types. An inspection of the list as given shows discoidal cleavage alongside of the holoblastic type in many of these groups. The myxinoids are discoidal while the lampreys have holoblastic cleavage in the class Cyclostomata. Among the fishes, elasmobranchs and teleosts are extremely disceidal, but the dipnoid and the ganoid fishes are holoblastic in type. The typical amphibian egg is holoblastic, but ‘the Gymnophiona show discoidal cleavage. Instead of having taxonomic significance, the distribution of discoidal cleavage is related entirely to the amount of yolk present in the egg.


The relationship between the holoblastic and ineroblastic types of cleavage will be best understood by recalling the cleavage of the frog egg (figs. 22 and 26). From the condition found in the frog egg we may pass by a consideration of the cleavage of /icipenser, the sturgeon, Amia, the bowfin, and Lepidosteus, the gar pike, to those found in the tcleost egg. That is, we pass from the telolecithal egg of the amphibian or lamprey by increasing degrees of separation of yolk and protoplasmic portions to the nieroblastic type of the modern tcleost.


l*'I<.. 44. A, ('l(‘.l\:U.EL‘ slag!-\ of the sturgeon .l(i;unxu zulhcnus, B, section through ~mme. (l{e(lr'.u\'n from Ziegler, after Whiunan and E_v(-leshymer.)

The cleavages of the lamprey and of the frog show remarkable similarity. In both there is a large proportion of yolk, but it is still suffieiently separated into spherules for the cytoplasm to cut cntirelv through it. Cleavage is total and unequal, the first two furrows being meridional and separating the eggs into four blastomeres. The third furrow is latitudinal. In Petromyzon the fourth furrows mark the beginning of irregularities in cleavages whereby the cells of the animal half cleave more rapidly than the vegetative half, some of the furrows not being completed until very late.


In the sturgeon, according to the description of Dean, the first cleavages separate the blastomeres but do not penetrate deeply into the yolk. The egg in the late segmentation stages shows a protoplasmic cap of small cells of irregular size and outline. Horizontal cleavages have also occurred and meridional cleavages have separated off marginal cells in an irregular manner so that the surface of the yolk half of the egg becomes subdivided into many-sized polygonal cells. While the protoplasmic cap of small cells constitutes a blastodisc, it does not include all the protoplasmic portion of the egg, as in the case of the true discoidal types. The cells adjacent to it are connected with the yolk. The blastedisc proper, however, is separated from the yolk by the cleavage cavity, the floor of which consists at first of a few irregular yolk-bearing cells. There is no sharp distinction between these cells and the yolk which they are doubtless helping to elaborate into nutritive supplies for the growing blastodisc. Obviously the blastula here, which consists of a. blastodisc grading into shallow cells covering the yolk mass and separated by the segmentation cavity from the yolk-laden cells beneath it, has points of marked similarity with the telolecithal type of the lamprey.


fiG. 45. A, B. cleavage stages of Potromyzon fluviatilis; C, D, cleavage stages of Primmyzon. plancri. (Redrawn from Ziegler, from Hatschek.)

The inner yolk-containing cells of the latter are not represented in the sturgeon, in the yolk of which no cell boundaries are to be distinguished although the outer polygonal cells of the yolk hemisphere possess dividing nuclei. The formation of the body of the embryo is more distinctly limited to the blastodisc in the case of the sturgeon.

The next step toward the meroblastic type is seen in Amia. Here the cleavage furrows begin much as in the previous cases but the furrows are more retarded in spreading over the egg surfaces. While at first the meridional furrows are making their way toward the opposite pole, four vertical furrows appear near the apical pole and extend downward. The next cleavage is the meridional one, cutting off thus a group of eight micromeres. At the next division these then divide into a superficial and a deeper segment and the macromeres divide by vertical furrows. A new latitudinal furrow cuts off additional micromeres and there is thus formed an apical disc limited to one end of the egg and much larger cell areas over the yolk portion; in the latter portion some of the developing furrows never become entirely completed. In Lepzdosteus the protoplasmic cap is still more sharply distinguished. The early furrows spreading downward over the egg’s surface never reach much


fiG 46 Cleavage of Amza calm (Redrawn from Ziegler, after Whitman and Eycleshymer )


beyond the equator so that the yolk hemisphele does not normally segment at all, that is, it more nearly attains the mcroblastic condition. The furrows which extend from the blastoderm over the yolk mass seem in later stages to disappear, and the protoplasmic layer in connection with the yolk contains numerous nuclei forming the so—called syncytium. These transitional stages bring us to the true discoidal cleavage as shown, for example, in teleosts. Eggs in which the distinction between the yolk and protoplasm is very sharply apparent have meroblastic cleavage, in the cases under consideration here, of the discoidal type. The first group of the vertebrates in which discoidal cleavage occurs is the Myxinoidae. Of the myxinoids the development of Bdellostoma is best known. It has been studied by a' number of investigators, notably by Doflein and by Dean. The egg is quite large, being in the neighborhood of an inch long and shaped something like a banana. It is well filled with dense yolk and the germinal disc is limited to one end. Its cleavage is very similar to that of the bony fishes which are shortly to be described. The first two furrows are approximately meridional, but irregularities begin with the direction of the third furrow and very shortly the arrangement of the furrows is that of a network enclosing the blastomeres. The outer cells are in continuation with the yolk and form a layer known as periblast. The divisions continue and the blastoderm comes to consist of several layers forming a cap covering the animal pole of the egg and gradually growing farther back over the egg. No blastocoele has been observed. The further development of the blastoderm is not entirely symmetrical, for the cells become more numerous on one side and on this side a separation of the thickened edge into two layers begins which represents the process of gastrulation in that

Fm 47 Egg of the gm PM the endoderm is separated off and with it Iaerndoetcue osemr»: In (leavaLt(' mesoderm. A gastrula cavity is not present.

Thus there is no definite end to the processes of cleavage and blastula formation after which gastrulation may be said to have begun, for the proliferation which permits the separation of the germ layers is entirely continuous with the cleavage processes. This type of development is seen to be totally different from that of the lampreys, which is so much like that of the amphibians as to require no special description.


So far as known all selachian eggs are extremely meroblastic and have discoidal cleavage. If a member of this group of fishes should be found with small holoblastie eggs, it would be a matter of considerable interest from the standpoint of the gradual adaptations which accomplish those modifications that are secondary to yolk accumulation. Dean has found a condition in the shark, Cestraczon, which suggests the approach of cleavage to the total, unequal type as described for Amw and Leprdosteus. Among the selachians are found genera which are viviparous as well as others which are oviparous. The former include, among others, the following genera: Hecvzmchus, N otodanus, Acanthias, Galeus, Squalus, M ustelus, Carcharias, and Torpedo. The egg-laying selachians include Scyllium, Pristiurus, Cestracion, and Raja. The oviparous species produce eggs enclosed in a horny characteristic shell oftentimes equipped with long processes by which they are attached to the water plants. The egg itself is spherical or ellipsoidal and consists of a germ disc lying upon a very large yolk mass. The yolk is of the consistency of a rather


fiG. 48. (‘leav-age stages of Bdelloslcmuz stouti. (Redrawn from Ziegler. after Dean.) A, B, 0. surface views; D, section through edge of blustoderm showing dorsal lip.

ropy liquid, pale yellowish with perhaps a greenish cast. Our knowledge of the early development of the selachian goes back chiefly to Ruckcrt.


In a number of selachians the fertilization process is completed and the fusion nucleus undergoes two mitoses before any cytoplasmic division is to be seen, although there are exceptions to this condition. The first furrow then makes its appearance as a slight groove across the disc and a second follows more or less at right angles to it. It is an interesting deviation from the expected sequence of events that oftentimes the second furrow corresponds to the first nuclear division. The divisions continue, and by the time the 16-cell stage has been reached the furrows separating the blastomeres form a network over the surface of the egg. fiG. 49. Cleavage of A. Torpedo ocellata (16 ce1ls), B, C, Scyllmm canicula. the dog shark (64 and 145 cells respectively) (Rod:-awn from Zwgler, nftu Ruchert)


The direction of the cleavage spindles in the fifth division is such that part of the cells are cut off under the others and of the 32 blastomeres, one sees at most only 20 to 24. In each case the peripheral divisions do not entirely cut off the corresponding cells but some remain in connection with the yolk by means of the continuous protoplasm which surrounds the blastodisc. The progress of cleavage now serves always to increase the number of free blastorneres and the cells below the surface likewise become. more numerous. For example, in a Torpedo, in which the blastodisc consists of 128 cells, it is said that about 70 of these are at the surface. In more advanced stages of cleavage the blastococle appears at first as a space beneath the growing disc. This completes the formation of the blastula.

fiG. 50. Sections through 16- 64-cell stages and through hlastoderm at the end of the cleavage period. (Redrawn from Ziegler, after Ruchert.)

In fig. C the posterior is toward the right, and tho blastoderm, cleavage cavity,bl., periblast cells, p., and supemumerary spermatozoa, 3., are shown.



fiG 51 Comparative diagrams of holoblastic and dlS(‘0ld'll eggs (Redrawn from Ziegler, after Boaz )

A, B, blastula and gastrula of the amphibian, C, D, blastula and gastrula of selachian


During the formation of the blastula there are to be observed around its edge, on the floor of the blastula cavity, nuclei scattered heie and there singly or in groups. These differ in appearance from the nuclei of the blastomeres, in that the chromatin is arranged in thicker masses and stains more darkly. They may be spoken of as yolk nuclei. The yolk nuclei are of double origin. The peripheral blastomeres which are in communication by means of a common circular band of protoplasm produce some of these yolk or periblast nuclei. The remaining yolk nuclei are derived from supernumerary spermatozoa which enter the egg at the time of fertilization. These yolk nuclei constitute a syncytium, a layer of protoplasm with scattered nuclei which surrounds the edge of the blastoderm and is continuous with the yolk. They are concerned with the nutritive changes involved in utilization of the yolk as food material. They disappear in the later stages and take no further part in the formation of the embryo proper.


The homology of the diseoidal type of cleavage as shown by the selachian and the holoblastic as shown by the amphibian is made clear by the accompanying diagrams from Boas. The blastula stages of the two show that the blastoderm of the selachian type is comparable to the small-celled animal half of the amphibian egg, a comparison which suggests the reason why the ectoderm of the amphibian is many-celled in thickness. In the amphibian egg the floor of the blastocoele is a mass of large yolk-filled cells; in selachians it is a layer of sub—blastocoele endoderm covering the yolk sphere and the scattered periblast nuclei. The linings or the floor coverings of the blastocoeles in the two cases are homologous, and periblast plus yolk cells of the selachians is homologous to the large, yolk-filled endoderm cells of the amphibian. In the gastrula stage this homology is emphasized by the fact that the gastrular invagination takes place at a point which is the morphological equivalent of the hinder edge of the selachian blastoderm where also the gastrulation will occur in this form.


These comparisons serve to point out that there is much less of a distinction between the cleavage types of holoblastic and meroblastic eggs than seems to be the case upon superficial observation.


The cleavage of the teleosts has been described for a great many forms and there is in general a fairly close agreement in the details. The eggs show the most complete segregation of protoplasm and yolk of all the Vertebrates. Among the teleosts of the present day it is the rule that very large numbers of eggs are produced, and in line with this fact the eggs are uniformly small, varying‘ in size from that of a small pea to that of a pinhead. There are a few exceptions to this statement among some fresh-water fishes, and these, together with the sharp segregation of yolk and protoplasm, suggest that in ancestral forms the yolk may have been very much larger in quantity and the egg more comparable in size to that of a selachian or of a bird. In most selachians the yolk is spherical and the protoplasmic layer which before fertilization shows but very slight localization accumulates at one place as a distinct elevation, after the entrance of the sperm. During polar body formation and cleavage, the protoplasmic portion is sharply distinguished from the yolk, but with the growth of the blastodisc the separation becomes less marked and at length the germ layers completely enclose the yolk mass. The yolk itself is at first in the form of spherules, but at the time of fertilization these run together to form a single spherical mass of glassy transparency. In many eggs, oil droplets are to be noted within the yolk which are presumed to regulate the specific gravity of the egg during

Fig. 52. Diagram of teleost cleavage. (After Ziegler)

m., egg membrane, bl, blastodisc, ps., perivitellme space, 37., yolk; 0., Oil drople pb., perxblast.

development. In the great majority of marine fishes the eggs float ai the surface of the water during their early stages.

Except for the fact that the planes of cleavage are much more regular, the segmentation of the germinal disc of the teleost egg does not differ in principle from that of the other types having discoidal cleavage. The first two furrows are meridional, the first one appearing in the shorter diameter of the ellipse, the form assumed by the blastodisc with the beginning of cleavage. The third and fourth furrows are vertical, becoming arranged so that they are practically parallel to the first and second. Thus, it is the rule that in the 16~ce1l stage the teleost egg consists of four rows of four cells each. In section it is to be noted that the first furrows do not extend to the yolk, but a continuous basal layer of protoplasm is left between the cleaving blastoderm and the yolk. The blastocoele appears at the end of the fourth cleavage by the third and fourth furrows curving around in their deeper portions to meet the preceding division planes which were perpendicular to the surface. Thus the 32-cell stage consists of a layer of superficial cells and a deeper-lying layer.


fiG. 53 Cleavage and formation of the blastoderm of the sea bass, Scrranus strarws (Redrawn from Ziegler, after H B Wilson )

A, B, C, D, are surface views, E, F, sections


The next division results in the blastoderm becoming three-layered, and in the fourth another layer is added, while at the same time the superficial cells also become more numerous. In subsequent stages it is seen that the cells of the basal portion will divide less rapidly but with this exception up to the twelfth division the nuclei divide regularly. The basal, uncleaved protoplasm gives rise to the yolk syncytium, the nuclei dividing repeatedly without cell boundaries being cut off about them. The peripheral layer of protoplasm, the periblast, enclosing the yolk mass, is continuous with this basal yolk syncytium. As development progresses, the nuclei of this layer divide regularly and assume appear— ances which are characteristic of cells whose chief function is concerned with digestion of the yolk. Multiple mitoses are observed, nuclei become numerous, are strangely lobed, and present appearances which are unlike the nuclei of normal cells but are understood when it is realized that their function requires immensely increased surface area. The cleavage cavity forms between the blastoderm and the periblast. The edges of the blastodisc thicken and gastrulation begins at a spot upon one edge of the blastoderm. The subsequent stages involve a gradual extension of the blastoderm over the entire yolk mass, steps which are concerned with the processes of gastrulation and subsequent development.


fiG. 54. Cleavage of the salmon, Salmo salar. (After Ziegler.) A, 16-cell stage; B, blastula.


The cleavage of the eggs of Gymnophiona are among those which show the discoidal type. The earliest stages have not been observed, but the egg and the later cleavage stages are so similar to those of birds and VERTEBRATES 89

reptiles, particularly of the former, that it seems unnecessary to devote space to that here. The student of general embryology is interested in them for the contrast which they present to other types of amphibian development.

The eggs of birds and reptiles are very much alike in all fundamental respects and resemble also those of the elasmobranchs. The amount of yolk present is large and the protoplasm and yolk are distinctly separated from each other, although the segregation is less sharp. The germinal disc is more intimately connected with the yolk and at its edges


fiG. 55. Cross sections through the germ disc of the teleost, Ctenolabrus. (Redrawn from Korschelt and Heider. after Agassiz.)

gradually passes over into yolk in distinction to the sharp line of separation noted in the teleosts. The eggs of birds have been studied by many investigators and the early stages are quite thoroughly understood. The general procedure is similar to that of elasmobranchs, but the early furrows are more regular, the first two being meridional and at right angles to each other. They are then followed by a pair of vertical furrows. The irregularities are many, however, and in certain species they occur earlier than in others. In the early cleavage of the chick, for example, Patterson found that the third cleavage furrows may not be clearly recognizable. Accessory sperms enter the eggs of birds, and the phenomenon known as accessory cleavage is due to an attempt at segmentation on the part of the yolk in which these accessory sperm nuclei come to lie. The attempt is transitory, however, and subsequently the partial furrows disappear and the nuclei degenerate. The first cleavages result in the formation of the central cells which are completely out off from the unsegmented protoplasxn, and of marginal cells which are still connected with the surrounding protoplasm. From the marginal cells new central cells are constantly cut off and new marginal cells arise peripherally. With the formation of the central cells, due to horizontal cleavages, a space is formed between them and the underlying protoplasm. This space becomes filled with fluid and is the segmentation cavity. In general the processes already described for the formation of discoidal cleavage in the lower vertebrates also apply to that in reptiles


fiG. 56. Periblast cells showing many mitoses from a. cleavage stage of Belone. (Redrawn from Ziegler, after Kopsch.)

and birds. For more detailed descriptions the reader is referred to such comprehensive accounts as those of the chick which are easily available.

III. IRREGULAR CLEAVAGE

In bringing to a close the sections dealing with cleavage it is necessary to mention certain irregular cleavages which do not fall in any of the classes previously discussed, or at least are so modified that their relationships have not yet been certainly made out. The cleavages of some sponges and of some coelenteratcs, though undoubtedly fundamentally radial, present variations from the normal type that are so great as to be understood only with difficulty. The cleavages of the trematodes and cestodes are among the most irregular of all forms. The cleavages of brachiopods and of bryozoans, although total and equal, do not follow the usual pattern. In most of the cleavage classes discussed an occasional irregular case is also to be found. Perhaps further work will bring many of these into line with the more regular forms.

Bibliographic Note

Among the more important accounts of the subjects contained in this chapter are the following: Superficial: Brauer, Korschelt and Heider, Bigelow, Heider on Hydrophilus, Cano; Cephalopods: Watase, Vialleton; Vertebrates: Dean, Whitman and Eycleshymer, H. V. Wilson, Agassiz, Kopsch, Patterson. 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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