Russell1930 13

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Russell ES. The interpretation of development and heredity. (1930) Oxford. Univ. Press.

   The interpretation of development and heredity (1930): 1 Introductory | 2 Aristotle’s ‘De Generatione Animalium’ | 3 Preformation and Epigenesis | 4 The Germ-Plasm Theory | 5 The Theory of the Gene | 6 Some Modern Epigenetic Theories | 7 Wilhelm Roux and the Mechanics of Development | 8 The Mnemic Theories | 9 Retrospect. The Use and Misuse of Abstraction | 10 The Organismal Point of View | 11 The Physiological Interpretation of the Cell Theory | 12 The Cell and the Organism | 13 The Cell in Relation to Development and Differentiation | 14 The Organism as a Whole in Development and Reproduction
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XIII The Cell In Relation To Development And Differentiation

Like the Protozoon, the animal ovum is by definition a cell, but — also like the Protozoon — it is in addition an organism and not merely a cell. It is the organism in its earliest stage, when it is small and monoenergid. When the ovum segments it still remains one organism, with the sole change that it has become polyenergid, and as a rule multicellular. There is direct continuity from the unsegmented ovum right up to the adult organism. It is true that in many cases the segmentation-spheres appear to be spatially distinct, 1 and single blastomeres may have the power when isolated of reproducing the whole organism. But there are also many cases, e.g. in Arthropods, where separate blastomeres are not formed at first, and the embryo remains for some time plasmodial.

Under the influence of the cell-theory, the simple fact of organic continuity from ovum to adult has been rather overlooked, and too much stress laid on the multiplication of cells during early ontogeny. It has been considered that segmentation is essentially a process of duplication and re-duplication of that which is accepted as the fundamental biological unit — the cell, and that differentiation is based upon cell-multiplication.

It is to Rauber 2 in 1883 that we owe the restatement of the obvious truth that in spite of cell-multiplication the organism is and remains one unity from the earliest to the latest stages of its development, and that accordingly the unsegmented egg is not merely a cell but a unicellular or monoenergid organism.

1 Intercellular connexions between blastomeres have been observed in echinoderm and nemertine eggs (Refs, in Wilson, 1925, p. 106).

2 Morpb.Jabrb. viii, 1883, pp. 233-338.

The living thing is not constructed as is a house or a factory, by the adding together in an orderly way of one building-stone after another; its unity and primary plan are there from the beginning, so that the organism is from the beginning a whole, from which by self-differentiation the parts are derived 1 (p. 308). In this sense the whole determines the parts, not the parts the whole.

‘For the finished organism is nothing else than the fertilised egg which has increased and divided in an orderly way. The determining conditions of the type of growth are contained in the egg, as are also those of its division. The fertilised egg is the whole in its youngest state. The first two segmentation spheres, into which it divides, derive all that they are from their source, the egg. What is true for the first two parts holds good for all the rest — they are determined according to the laws which presided over their first beginnings* (p P . 313-14).

From which we get the following definition of the developing organism: it is ‘a protoplasmic body which increases in size in definite directions, divides itself up in the different dimensions of space, and differentiates itself in orderly fashion chemically and histologically’ (p. 332). The cells into which it divides are of subsidiary and minor importance in comparison with the developing organism as a whole, and they are in no sense elementary units, or ‘elementary organisms’.

In the same year as Rauber, Sedgwick wrote with reference to the syncytial development of Peripatus, ‘if these facts are generally applicable embryonic development can no longer be looked upon as being essentially the formation by fission of a number of units from a single primitive unit, and the co-ordination and modification of these units into a harmonious whole. But it must rather be regarded as a multiplication of nuclei and a specialization of tracts and vacuoles in a continuous mass of vacuolated protoplasm’. 2 Sedgwick accordingly, like Rauber, took the organismal rather than the analytical view of development.

The same point of view was brilliantly stated by Whitman 3

1 The parts are the way in which the whole organizes itself— a phrase which I owe 0 Mr. R. G. Collingwood (in litteris).

2 Quoted in his paper of 1885, already referred to.

2 C. O. Whitman, ‘The Inadequacy of the Cell-Theory of Development’, Wood's Holl Biological Lectures for l 8 gj y Boston, 1894, pp. 105-24.

in his famous lecture on the cell-theory. He maintained, and supported his contention with a wealth of illustration, that the organization of the embryo and the adult is independent of the manner of its subdivision into cells. ‘The plastic forces heed no cell-boundaries, but mould the germmass regardless of the way it is cut up into cells’ (p. no). The organism is an organism from the egg onwards, and continuity of organization is the essential thing in development, division into cell-territories being entirely secondary. ‘Continuity of organization does not of course mean preformed organs, it means only that a definite structural foundation must be taken as the starting-point of each organism, and that the organism is not multiplied by cell-division, but rather continued as an individuality through all stages of transformation and subdivision into cells’ (p. 112).

With this typical organismal or integral view of development he contrasts the colonial, elementalist conception, which was then widely held.

‘While all will admit that the organization of the egg is such as to predetermine the organism, few will be prepared to admit that the adult organization is identical in its individuality with that of the egg. The organism is regarded rather as a community of such individualities, bound together by interaction and mutual dependence. According to this view, development does not consist in carrying forward continuous changes in the same individual organization, but in multiplying individualities, the complex of which represents, at every stage, not the organism, but one of an ascending series of organisms, which is to terminate in the adult form.’ 1

‘In the egg-cell we are supposed to have an elementary organism; in the two-cell stage, two elementary organisms, forming together an organism of a totally different order, based on a new scheme of organization. In the four-cell stage we have another organism, in the eight-cell stage another, and so on’ (pp. 1 13-14).

1 That this is not an exaggerated statement of the elementalist position is shown by the following passage quoted in translation from Hertwig by E. B. Wilson {Wood's Holl Biological Lectures for 1893 , p. 8 ): ‘The egg is an organism which multiplies by division to form numerous organisms equivalent to itself, and it is through the interactions of all these elementary organisms, at every stage of the development, that the embryo, as a whole, undergoes progressive differentiation.*

This view, he holds, is totally incorrect. The unity of the organism is not a secondarily acquired unity, it is there from the beginning of development — fundamental organization precedes cell-formation in time and regulates it, rather than the reverse.

‘We must look entirely behind the cellular structure for the basis of organization. Even a highly differentiated organism may reach a relatively late stage of development j ust as well without cell-boundaries as with them, as we see so well illustrated in the insect egg. If we fall back on the number of nuclei as the essential thing, then we shall have to reckon with multinucleate infusoria. In these forms do we not see that it is always the same organism before us, as we follow its history through the whole cycle of nuclear phases ?

‘The essence of organization can no more lie in the number of nuclei than in the number of cells. The structure which we see in a cell-mosaic is something superadded to organization, not itself the foundation of organization. Comparative embryology reminds us at every turn that the organism dominates cell-formation, using for the same purpose one, several, or many cells, massing its material and directing its movements, and shaping its organs, as if cells did not exist, or as if they existed only in complete subordination to its will, if I may so speak’ (p. 119).

It is a curious fact, to be explained no doubt by the strength of the particulate conception in his time, that Whitman considered the ground of assimilation, reproduction, and regeneration, in short of all the fundamental vital functions, to lie in ultra-microscopic idiosomes, whose action and control were of course not limited by cell- boundaries (p. 123). The idiosomes were the bearers of heredity and the real builders of the organism — the determining agents of organization and differentiation. But clearly, organization can no more be explained by the properties of the individual idiosomes than the unity of the organism can be explained from the properties of its constituent cells.

If Whitman had applied to the idiosomal conception the same criticism which he used with such effect against the cell-theory, he would have been convinced of the total inadequacy of this conception also.

Dobell, in the paper to which we referred in the last chapter, contrasts the segmentation of the Metazoan ovum with the multiplication of the Protozoan individual. He writes :

‘A metazoan egg undergoing segmentation is a non-cellular organism undergoing differentiation by forming cells. Before segmentation the egg is a whole organism ; after segmentation it is the same whole organism, but more differentiated. After segmentation, the organism is not a colony of individuals each of the same value as the original egg. A protozoon undergoing division, on the other hand, is one organism dividing into two; it is one whole organism becoming two whole organisms of the same value as the original whole organism. If segmentation were really analogous to the divisions of a protozoon, it would produce a cluster of eggs and not a differentiated organism’ (p. 302).

Frank Rattray Lillie (1870 – 1947)
Frank Rattray Lillie (1870 – 1947)

In stating recently the fundamental concepts of the physiology of development, F. R. Lillie 1 gave a prominent place to the principle of ‘individuation’.

‘The germ’, he wrote, ‘is physiologically integrated as an individual at all stages. It may be first merely a cellular individual, then a definitely polarized individual with one or more axial gradients; as development proceeds, specific correlations, including those of definitely nervous and chemical natures, make their appearance. In short, the physiological principles upon which integration depends undergo differentiation, in the sense of progress from relatively simple and few to relatively complex and many, during development. While individuality may thus appear to grow, it is in reality complete at all stages, only the means to its realization changing and multiplying with growing complexity’ (p. 362).

A good example of the organismal conception of development ! Lillie expressed this same view of the essential unity of the developing organism even more clearly in an important paper written some twenty years previously , 2 in which the following striking passage occurs :

‘If any radical conclusion from the immense amount of investigation of the elementary phenomena of development be justified, this is; that the cells are subordinate to the organism, which produces them, and makes them large or small, of a slow or rapid rate of division, causes them to divide, now in this direction, now in that, and in all respects so disposes them that the latent being comes to full expression. We see this in the adaptiveness of the process of cleavage of the ovum, in the regeneration of a starving planarian constantly suffering a diminution in the number of its cells while its structure is increasing in complexity, in “regulation”, and in all cases of morphallaxis, whether in a protozoan or a metazoan. The organism is primary, not secondary; it is an individual, not by virtue of the cooperation of countless lesser individualities, but an individual that produces these lesser individualities on which its full expression depends’ (p. 252).

1 ‘The Gene and the Ontogenetic Process*, Science , lxvi, 361-8, 1927.

2 ‘Observations and Experiments concerning the Elementary Phenomena of Embryonic Development in Cbaetopteru$\ Journ . Exper . ZooL iii, 1906, pp. 153268.

This principle of unity, or action of the organism as a whole, corresponds to Whitman’s concept of organization. It is prior to visible differentiation, and is a ‘property of the whole distinct from the discernible properties of the parts’ (p- 253) The same view, that development is essentially an activity of the organism as a whole, has also been upheld by others — by Conklin and Child for instance, and by Ritter, as we have seen in earlier chapters.

2. The argument from the continuity of development is sufficient in itself to show that the ovum is not merely a cell but the future organism in its simplest state. But there is in addition a good deal of evidence which indicates that in many groups the fertilized but unsegmented egg is already differentiated as a whole, in such a way that particular areas of its substance represent and give rise to particular organs and organ-systems of the adult — I refer of course to the facts of ‘germinal localization’. We shall see more clearly in considering these facts that development is essentially a process affecting the organism as a whole, that the organism develops as a unity from its earliest beginnings right up to maturity and old age, and that cell-division and even nuclear division are events ancillary and adjuvant to the main developmental process, not primary and fundamental events in terms of which that process can be fully expressed.

We shall see that the ovum is essentially a monoenergid organism which differentiates its substance progressively, and becomes by reason of its increase in size polyenergid, and as a rule multicellular. The story of early development, as revealed by the able experimenters of the last thirty years, provides us in fact with a clear demonstration of the necessity for a synthetic or organismal treatment of development, and of the complete inadequacy of the analytic view.

It is to W. His in 1874 that we owe the first suggestion of organ-forming areas in the germ (see above, p. 95 f.n.), but the seed fell bn stony ground, and was stifled by the upgrowth of speculation on the part played by the nucleus in differentiation, which followed the brilliant cytological discoveries of the early ’80s. Experimental embryologists, under the influence of the cell-theory, at first paid attention chiefly to the fate of isolated blastomeres and groups of blastomeres, and it was not till near the end of the century that they discovered the existence of ‘organ-forming substances’ located in definite areas of the egg-cytoplasm. Some years later, the theory of germinal localization took shape, particularly from the hands of Wilson and Conklin.

It is unnecessary here to follow up the steps by which the theory was established, the more so because the whole fascinating story is told by Wilson with a competence and authority that cannot be rivalled. 1 For our purpose it is sufficient to single out a few typical cases in support of our contention that the egg is already at a very early stage the organism-to-be.

In the first place we may recall those cases where the egg shows the same orientation and symmetry as the future organism. This is true of many insect eggs, which have an anterior and a posterior end, dorsal and ventral surfaces, and a right and left side, which correspond with these aspects in the adult. The egg of the cuttlefish, Loligo, also shows definite bilateral symmetry.

Wilson, 1925, Chapters XIII and XIV.

Edwin Grant Conklin (1863 – 1952)
Edwin Grant Conklin (1863 – 1952)

For more detailed evidence of germinal localization we must however turn to those eggs that exhibit ‘mosaic’ cleavage, of which many examples are known among Mollusca, Annelida, and Ascidians. As a typical case we may take the ascidian Styela, so thoroughly investigated by Conklin. In the egg of Styela germinal localization is not established until maturation and fertilization take place. In the egg before maturation there is visible only a central grey yolky mass, surrounded by a superficial layer containing yellow pigment. When the germinal vesicle breaks down to form the first polar spindle, a clear substance is liberated which later forms the ectoderm of the larva. Further localization is dependent on the entrance of the sperm. When this happens, the yellow superficial plasm collects at the lower pole of the egg, where the sperm enters, forming a yellow cap.

‘This yellow substance then moves, following the sperm nucleus, up to the equator of the egg on the posterior side and there forms a yellow crescent extending round the posterior side of the egg just below the equator. On the anterior side of the egg a gray crescent is formed in a somewhat similar manner, and at the lower pole between these two crescents is a slate blue substance, while at the upper pole is an area of colorless protoplasm. The yellow crescent goes into cleavage cells which become muscle and mesoderm, the gray crescent into cells which become nervous system and notochord, the slate blue substance into endoderm cells and the colorless substance into ectoderm cells. Thus within a few minutes after the fertilization of the egg, and before or immediately after the first cleavage, the anterior and posterior, dorsal and ventral, right and left poles are clearly distinguishable, and the substances which will give rise to ectoderm, endoderm, mesoderm, muscles, notochord, and nervous system are plainly visible in their characteristic positions.’ 1

The monoenergid egg of Styela is therefore, immediately after fertilization, a rough model of the future organism; its subsequent development consists in a further differentiation of the organ-systems already mapped out, accompanied by an increase in size.

While in Styela and in many other forms definite localization of special cytoplasmic areas does not take place before fertilization, it is to be noted that this is not an invariable rule. In some forms, e.g. Myzostoma and Dentalium, a definite zoning of ‘formative substances’ is established even before maturation. As Wilson points out, the history of development does not commence with fertilization — there is an epigenetic differentiation of the ovarian egg, leading up to the stage at which it can be fertilized, or otherwise stimulated to begin the development of a new organism.

1 E. G. Conklin, Heredity and Environment , 2nd edit., Princeton, 1916, pp. 123-4.

While the Ascidian is the type in which germinal localization is most detailed and most clearly visible, the state of affairs which we have described for Styela is parallelled in greater or less degree in most of the great groups of the animal kingdom.

‘There are types of localization of these cytoplasmic materials in the egg which are characteristic of certain phyla; thus there are the ctenophore, the flat-worm, the echinoderm, the annelid-mollusk and the chordate types of cytoplasmic localization. The polarity, symmetry and pattern of a jellyfish, starfish, worm, mollusk, insect or vertebrate are foreshadowed by the characteristic polarity, symmetry and pattern of the cytoplasm of the egg either before or immediately after fertilization. In all of these phyla eggs may develop without fertilization, either by natural or by artificial parthenogenesis, and in such cases the characteristic polarity, symmetry and pattern of the adult are found in the cytoplasm of the egg just as if the latter had been fertilized’ (Conklin, ibid., pp. 181-2).

For our second example we may take the egg of the frog, which shows, immediately after fertilization, a structure foreshadowing that of the adult, though not visibly in such detail as does the egg of Styela. We shall follow the admirable account given by Brachet, 1 who has himself contributed so much to the elucidation of the first steps in the development of this much studied form.

In the ripe but unfertilized egg of Rana fusca ( = R. temforarta) there is no trace of bilateral symmetry. There exists of course a radial symmetry, and a differentiation of the animal from the vegetative pole. Such polar symmetry is almost universal in animal ova, and has as a rule a very definite prospective significance, since the substance of the animal pole generally gives rise to the ectoderm and its derivatives, that of the vegetative pole to the endoderm. In

1 A. Brachet, L'CEuf et Us Facteurs it VOntogenese , Paris, 1917.

the egg of Rana, before fertilization, there is no specific localization of potentialities ; destruction of a small area of the cytoplasm of the egg does not lead to a specific defect in the embryo, provided the operation is carried out before, or shortly after, fertilization. Up to about 45 minutes after fertilization, germinal localizations either do not exist, or if they have been formed, they are unstable and labile, and the egg can still regulate and re-arrange them. When more than an hour has passed, local injury to the cytoplasm entails the absence in the embryo of the part to which this locus of the cytoplasm normally gives rise — the egg has become definitely and irrevocably a mosaic of potentialities of a generalized character. This organization and fixation of elementary structure is in the frog normally brought about by the entrance of the sperm, and reaches its term at the moment when fusion of the male and female pronuclei takes place. About two hours after fertilization a visible external sign of the organization of the egg becomes apparent in the shape of the grey crescent, which forms at one side between the pigmented upper hemisphere and the lower white hemisphere. The grey crescent is invariably directly opposite the point of entrance of the sperm ; it marks the plane of bilateral symmetry which is now established in the egg; and this plane becomes invariably the plane of symmetry of the embryo and the adult. The dorsal lip of the blastopore, which acts as a centre of growth and differentiation, takes its origin from the broadest part of the crescent.

We see then that shortly after fertilization the main lines of the future organization are laid down in the unsegmented

egg When the egg is artificially fertilized, as can be done by pricking it with a needle, the formation of the grey crescent takes place normally, and the egg organizes its structure, though there is no relation between the position of the prick and the point of appearance of the grey crescent. The establishment of bilateral symmetry and of the main lines of organization is then clearly independent of any specific organizing action of the male pronucleus.

The localization of specific potentialities in the unsegmented egg of Rana is not so detailed and definite as in Styela, or at least is not so easily demonstrable; the frog’s egg therefore occupies an intermediate position between typically mosaic eggs and the so-called regulative eggs, in which germinal localizations are much less definite and much less stable. As an example of the regulative type we may take thoegg of the sea-urchin Paracentrotus (Strongylocentrotus) lividus, investigated by Boveri. This egg shows a horizontal band of pigment lying below the equator, separating the top white hemisphere from a bottom white cap. The upper hemisphere gives rise to ectoderm, the pigmented zone to the archenteron, and the bottom cap to mesenchyme. But the separation of the three substances is not very strict, as is shown by the potency of the isolated blastomeres. The first two divisions are meridional, and all four blastomeres receive samples of the three strata of the egg. Each of these four blastomeres when isolated gives rise to a complete larva. The third cleavage plane is equatorial, and establishes a difference between the upper and the lower quartet of cells. In spite of this, however, gastrulae can be obtained from the isolated cells of this stage, but less frequently and less completely from the cells of the upper quartet. The egg showing the least degree of cytoplasmic localization is that of the hydromedusan studied by Zoja, which shows a concentric grouping of substances, such that each of the first sixteen blastomeres receives an equal share, and is accordingly able to produce when isolated a complete small larva. In these eggs, as in the sea-urchin’s, bilateral symmetry and the main plan of the future organization are established at a later stage than in the more precocious eggs of Styela and Rana.

3. We may now consider the relation of cleavage or segmentation to the egg-pattern in these different types. We note, first of all, that at least up to the blastula or corresponding stage, the process of cleavage adds nothing to tlyj original organization of the egg — it merely divides up the substance of the egg in a more or less stereotyped way. In the blastula the same differentiated cytoplasmic regions can be discerned, occupying the same positions relative to one another as in the unsegmented egg. 1 The localization of substances is the same in the blastula as in the fertilized ovum.

The relation of the cleavage-pattern to the fundamental organization of the egg is different however in the various typical forms we have considered. In Styela the cleavagepattern is modelled upon the egg-pattern, following it closely in such a way as to separate off progressively the differentiated substances of the egg-cytoplasm.

‘At the first cleavage of the egg each of these substances is divided into right and left halves. The second cleavage cuts off two anterior cells containing the gray crescent from two posterior ones containing the yellow crescent. The third cleavage separates the colorless protoplasm in the upper hemisphere from the slate blue in the lower. And at every successive cleavage the cytoplasmic substances are segregated and isolated in particular cells, and in this way the cytoplasm of the different cells comes to be unlike. When once partition walls have been formed between cells the substances in the different cells are permanently separated so that they can no longer commingle’ (Conklin, 1916, p. 125).

In such typically mosaic eggs, the first cleavage plane stands in a fixed relation to the plane of bilateral symmetry, and the subsequent cleavages separate off progressively the specific areas already differentiated in the cytoplasm of the egg. It comes about then that from the very beginning the individual blastomeres are different from one another, each being specialized for a particular destiny. They are in a measure like tissue cells — specified as to type and fate. We can understand therefore why, if one of the first two blastomeres is killed, the surviving one develops into a half embryo, and not a whole one, and why cells isolated at a later stage (as can be done in the mosaic eggs of some Gastropods) produce only that part of the larva to which they would have given rise normally. The classical case is that of the Ctenophore Beroe , in which isolated blastomeres of the 2-cell, 4-cell, or 8-cell stages produce partial larvae,

1 Ih illustration of this, see for example Figs. 512 and 513 in Wilson, 1925, and Figs. 6, 9, 10, and 27-9 in Conklin, 1916.

fractions of the whole, possessing respectively 4, 2, or 1 of the normal 8 swimming-combs. The same type of result can be obtained by operating on the unsegmented egg — larvae showing specific defects are obtained.

The relation of cleavage to egg-pattern in the frog’s egg is particularly interesting. Here the first cleavage plane may, or may not, coincide with the plane of bilateral symmetry established by the entrance of the sperm. In about 70 per cent, of cases it coincides roughly with the plane of eggsymmetry; exact coincidence is found only in 40-50 per cent, of cases according to Brachet. The two planes may in fact form any angle with one another, but there is a distinct bias towards coincidence. If one of the first two blastomeres is killed the remaining one gives rise to a partial embryo, and the composition of this partial embryo depends upon the relation of the first cleavage plane to the bilateral plane of the egg. If the two planes approximately coincide the result will be a half embryo — right or left as the case may be. If the first cleavage runs transversely across the egg, and the posterior blastomere is destroyed, the anterior blastomere gives rise to an embryo complete as to its front half but dwindling off towards the tail. In general, the fate of the surviving blastomere depends upon how much of the grey crescent it contains (Brachet). The interesting point for us is that there is no necessary relation between the direction of the cleavage planes and the fundamental structural plan of the egg. As Brachet puts it, ‘In the fertilized egg of the frog, whatever may be the orientation of the first cleavage plane relatively to the plane of bilateral symmetry, the latter maintains itself completely throughout the whole course of development; all the parts and all the primordial organs of the embryo are formed in positions determined by the material and dynamical constitution of the egg’ (1917, pp. 266-7).

We must note in passing that though in the frog as a rule only partial embryos appear after the destruction of one of the first two blastomeres, it is possible by suitable manipulation to obtain a whole embryo of small size from each of the two • — the mosaic character of the egg is not so rigid as in Styela.

Turning now to the egg of Paracentrotus, we find that the germinal localizations are not so precise and stable as in Styela and the frog. The symmetry of early development is radial, and the main differentiation is polar. As we have already seen, the first four blastomeres when isolated can give rise to complete larvae, and the same holds good to some extent for the first eight.

It is now generally accepted that the difference between ‘mosaic’ eggs and ‘regulative’ eggs is no absolute one, but depends (i) upon the degree of cytoplasmic differentiation reached by the time the egg is capable of fertilization, and on the degree of organization imposed upon the egg by fecundation, and (2) upon the varying regulative power of the egg, which enables a part of it to re-arrange its structure so as to produce not a part but a complete larva of reduced size. Eggs such as that of Styela are, as it were, precociously advanced at the time of fertilization, and it is a fact of much significance that with this good start they run through their larval development with great rapidity, reaching the fully formed ‘tadpole’ stage in 12 hours. Correlated with a highly developed mosaic character of the egg there is generally a lack of regulative power, so that parts of the egg give rise only to partial embryos. The frog’s egg is not so advanced in development and has farther to go after fertilization; it has a certain degree of regulative capability. The sea-urchin egg is less advanced still, and quite small fractions of it can reconstitute the whole. It must be remembered that the development of the egg does not begin with fertilization; there is a long period of ovarian growth, during which there is not only a nuclear but also a cytoplasmic maturation. Having regard to the occurrence of natural parthenogenesis and the comparative ease with which artificial parthenogenesis can be induced, we may regard fertilization as an incident — important but not essential — in the course of the development of the egg from its earliest beginnings up to the finished form.

With respect to segmentation also, there is a broad difference between the two classes of eggs, for segmentation is generally determinate in mosaic eggs, having a close relation to the already established promorphology of the egg, while in regulative eggs this relation is much looser, or even nonexistent. The frog’s egg is very definitely transitional between the two. Considering the facts as a whole, we see one point emerge clearly — that there is no necessary connexion between segmentation and differentiation. From a theoretical point of view, the two things are quite distinct. The two processes may in certain cases coincide and reinforce each other, as in the determinate cleavage of mosaic eggs, but this fact cannot be generalized. Both in the mosaic and the regulative egg, segmentation is in reality nothing more than a fragmentation of the substance of the egg; what each blastomere contains depends entirely on its position in relation to the initial structure of the egg as a whole. As Brachet puts it, the fate of each blastomere is determined by the quality and the quantity of the materials which it contains, by those materials which have fallen to its lot as a consequence of the particular mode of segmentation of the fertilized egg (p. 269). Segmentation adds nothing to the original diversity of the egg, though it may help towards further differentiation by segregating specific substances from one another. The egg after fertilization is a mosaic of potentialities which have their seat and substratum in the germinal localisations. At the beginning of its development, the egg, in segmenting, divides up into cells (blastomeres) which become progressively smaller and more numerous. So long as no notable displacement occurs of the blastomeres formed, one must consider segmentation as equivalent to a simple division ( decoupage ), and each blastomere, in virtue of the germinal localisations of the egg, has its destiny fixed for it by its individual composition. Experiment proves . . . that this dividing up of the egg may take place in quite a different manner from that demanded by the normal laws of segmentation, without the final result of development being altered’ (Brachet, p. 192).

The reference in the last sentence is to the well-known experiments on the eggs of sea-urchins and the worm Nereis , in which by means of pressure the normal course of cleavage is upset, without affecting the normality of the result. 1

In sum:

‘Segmentation ... is purely and simply a fragmentation {morcellement) of the egg, and has by itself no formative value whatsoever. It creates no new germinal localisations, it does not shift those that exist, and it does not interfere with the bilaterally symmetrical organisation of the egg. The only new fact that appears during its course is that the regional potentialities, in the measure in which they become progressively isolated in particular blastomeres, become more fixed and more stable, and take on a more and more definite determinative character; the mosaic composition of the egg, which is sometimes difficult to discover at the beginning, becomes more definite and precise as segmentation proceeds’ (Brachet, p. 259 ).

Before going on to consider a point which arises naturally out of the preceding discussion, namely the rationale of segmentation, it is desirable to say something about the ‘organ-forming stuffs’ which characterize the differentiated regions of the mosaic egg.

It is now recognized that the visible substances — pigment, yolk, and so on — that can be distinguished in the egg may have nothing to do with differentiation, since they may be displaced by moderate centrifuging without interfering with normal development. The initial organized structure of the egg, which dominates all subsequent development, is more probably carried by the ground substance of the egg (the hyaloplasm) and the cortical layer. For, while mere shifting of visible organ-forming substances does not upset normal development, ‘by very strong centrifuging different areas of the cytoplasm itself . . . may be dislocated, and in such cases development is never normal; even the cleavage cells are atypical in form and position as well as in contents and each of these different kinds of cytoplasm, if it develops at all, gives rise to its own specific part or organ in the larva wherever it may be located. In this way the most bizarre monsters may be formed, with their different organs out of all proper relation to one another.’ (p. 19). 2

1 See Wilton, 1925, pp. 1059-62.

2 E. G. Conklin, ‘Problems of Development*, American Naturalist , lxiii, 1929, pp. 5-36,

From the organismal point of view, the so-called ‘organforming’ substances can of course have no actual formative powers — their sole significance is as visible indices of the fundamental promorphology of the egg which is prior to segmentation and determines the first stages of differentiation. It is this initial organization ‘as a whole’ that adds point to our contention that the egg is only incidentally a cell, but fundamentally the organism-to-be. The fact that the egg is a cell has generally been allowed to obscure the more important fact that it is an organism.

4. We have already in Chapter XI devoted some attention to the process of segmentation, with reference especially to the size-relations of the cells and nuclei concerned. We have seen that the egg is a relatively inert cell, with a large inactive nucleus. During segmentation the nucleus is divided up into smaller and smaller units, so that its surface increases considerably. The total mass of the egg does not materially increase up to the blastula stage, though there may be transformation of yolk into protoplasm, but there is synthesis of chromatin and an increase of total nuclear mass. Owing to the repeated division of the nuclear substance the total surface area of the nuclei increases at a much greater rate than the total nuclear mass. We interpret these facts to mean that the metabolic activity of the egg is much increased and facilitated by this splitting up of the egg-nucleus into smaller units. Segmentation may therefore be regarded as a preliminary to further differentiation — a preparation or provision of metabolic units of the most effective dimensions for the future elaboration of organs and tissues.

A somewhat similar view of the rationale of segmentation is taken by Brachet, who emphasizes the significance of the morula and blastula stages as the terminal points of this preparatory work of the egg. Referring to these stages, he writes:

‘Their significance consists especially in the fact that they prepare for subsequent differentiation by enabling the blastomeres to attain the normal cell-size of the species to which they belong. The egg is, in fact, a cell the cytoplasmic body of which is considerably hypertrophied; the karyoplasmic ratio is profoundly disturbed, and in order that it may be restored it is necessary that the egg should fragment into smaller and smaller cells. By the blastula stage this result is achieved, and one notes as a matter of fact that although cellular proliferation goes on with great intensity, the size of the cells no longer diminishes in any appreciable degree in the later stages. The size maintains itself at this norm, because from this moment onwards the egg takes up nutriment, either at the expense of substances derived from the exterior or by utilising its deutoplasmic reserves. The blastula then marks the end of a period, a sort of critical stage in the physiology of the embryonic cells. The simple fragmentation by which it arises finishes with it, and gives place to the more complex processes of ontogenetic differentiation’ (p. 268).

The morula and the blastula form a whole just as does the egg itself, for they are merely the egg divided up into suitable metabolic units.

‘During the subsequent course of development, the gastrula, the larva and the adult organism, notwithstanding the growing complexity of their structure, continue to form a whole, of which the parts, however diversified they may be, remain intimately associated. The small initial differences, of a quantitative rather than a qualitative order, become more pronounced in their effects and that for many reasons, but the correlations which lie at their base persist no less, and become even more accentuated’ (p. 305).

That segmentation — the actual splitting up of the egg into blastomeres — has really nothing to do with the early processes of differentiation, but at most merely fixes and renders more definite the pre-existent differentiation of the egg, is shown also by the fact that in many eggs, particularly of the Arthropoda, the fragmentation of the nucleus, preparatory to later differentiation, is achieved without a corresponding division of the substance of the egg. Take for instance the development of the Asellid crustacean Jaera , as described by McMurrich. 1 In the egg of this form up to the stage with 32 nuclei every cell is organically united with its neighbours, so that the whole embryo forms a syncytium.

‘As stated’, writes McMurrich, ‘this is a highly important fact, since we see from it that a separation of the protoplasm into distinct spherules, such as presumably occurs in cases of total segmentation, is not necessary in order that histological differentiation may occur. Indeed, such an idea might have been derived from what we know of forms like the infusoria, in which, notwithstanding the fact that they are unicellular, differentiation of the protoplasm into myophanes, for example, occurs’ (pp. 140-1).

1 J. P. McMurrich, ‘Cell-Division and Development’, Wood's Holl Biological Lectures for 1894, Boston, 1895, pp. 125-47.

Even in eggs which normally show complete segmentation, it is possible by artificial means to suppress cleavage and yet obtain a considerable measure of differentiation. This has been done in certain annelid and molluscan eggs, particularly by Lillie in the egg of the worm Chaetopterus . x Such unsegmented eggs undergo to a certain extent the differentiations characteristic of the normal embryo and may even give rise to ciliated larvae bearing some resemblance to the normal trochophore. Conklin has recently shown that even in an egg showing such a definite and determinate cleavagepattern as Styela some differentiation may take place even though cleavage is prevented. 2

I have recently found’, he writes, ‘that when cleavage is suppressed but nuclear divisions continue in the fertilised eggs of the ascidian, Styela partita, the typical localization of the cytoplasms peculiar to the ectoderm, mesoderm and endoderm, the typical peculiarities of the nuclei in these areas, and even some of the histological differentiations of the tadpole stage and of its metamorphosis, may sometimes appear. However, the localization of these plasmas takes place normally at the time of the first cleavage and is provided for before that event; it is therefore not dependent on cleavage’ (pp. 13-14).

5. Not only is the early differentiation independent of cleavage, but it is independent even of nuclear division. That there is no qualitative division of the nucleus in early ontogeny is now firmly established ; 3 the process is purely quantitative, and the resulting nuclei are all strictly equivalent.

1 F. R. Lillie, ‘Observations and Experiments concerning the Elementary Phenomena of Embryonic Development in Chaetopterus ’, Journ . Exper . Zool. iii, 1906, P p. 153-268. .....

E. G. Conklin, ‘Problems of Development', American Naturalist , lxiii, 1929, pp. 5-36.

1 See Wilson, 1925, pp. 1057-62.

It is unnecessary to detail the evidence for this conclusion, but one particularly striking observation of Spemann’s may be adduced. By passing a fine loop round the egg of the newt it is possible to divide it more or less completely in two. This operation can be performed on the fertilized egg in such a way that one half contains the zygote nucleus, while the other half contains none. The nucleated part goes on dividing while the enucleate part remains undivided. When 16 nuclei have been formed one is allowed to enter the nonnucleated part, which then proceeds to divide and may give rise to a normal embryo. In this case i/i6th of the zygote nucleus plus a half of the protoplasm still contain all the elements for the formation of a normal embryo, and the system is capable of differentiating itself correctly (p. 187). This result is obtained only if the division of the egg has been into right and left halves ; if the constriction is frontal 1 /8th of the original nucleus is necessary to bring about development in the dorsal half. 1 The experiment demonstrates clearly that i/8th or i/i6th of the original nucleus differs from it only in size.

A quantitative nuclear division is found universally in the earliest development of all Metazoa, and we have seen what its probable physiological significance is. It might be expected that if nuclear division were prevented development would be rendered difficult or impossible, owing to the disturbance of the normal surface relations of the nuclei with the cytoplasm. Nevertheless, there is at least one case definitely known where embryonic development can go on (to a certain extent only, and in a somewhat abnormal way), while the nucleus remains undivided, increasing in bulk and in number of chromosomes, but not splitting up into daughter nuclei. This is the case of Chaetopterus , fully investigated by F. R. Lillie. 2 By treatment with potassium chloride not only cleavage but even nuclear division can be inhibited in the eggs of this form. Differentiation however goes on, though slowly; the characteristic distribution of substances in the

1 H. Spemann, ‘Vercrbung und Entwicklungsmechanik’, Zts. indukt. Abstain mungslebre , xxxiii, 1924, pp. 272-93.

2 Op. cit., 1906.

egg takes place, and the ectoplasm grows over the endoplasm to form a ‘unicellular gastrula’. The embryo develops cilia and swims actively about, and in some cases closely resembles the normal trochophore. Lillie summarizes the results of the differentiation of the uninucleate egg as follows :

‘(1) Organs are never formed, but only such structural elements as may occur in single cells of the trochophore. (2) Organs may, however, be simulated by the aggregation of the characteristic matter of an organ, for instance in the case of the yellow endoplasm, which simulates the gut of the trochophore, or the row of large vacuoles situated near the upper margin of the yellow endoplasm which simulates the row of vacuoles of the prototroch. (3) The structural elements appear in the same order of time as in the trochophore. (4) The distribution of structural elements tends to resemble that of the trochophore. (5) The yellow endoplasm (yolk?) is used up, apparently for the maintenance of metabolism, in the ciliated unsegmented eggs precisely as in the larva. (6) The apical flagellum is never formed’ (p. 237).

The case is a very important one, for it establishes clearly the possibility of a considerable amount of embryonal differentiation without either nuclear or cytoplasmic division. ‘This in itself’, Lillie points out, ‘is a fact of considerable importance, for it disposes effectually of all theories of development that make the process of cell-division the primary factor of embryonal differentiation, whether in the form of Weismann’s qualitative nuclear division, or of Hertwig’s cellular interaction theory’ (p. 245).

6. Summing up the results of our discussion regarding the early stages of embryonic development, we may conclude that the egg is essentially the organism-to-be, and only incidentally a cell. Differentiation is to be looked upon as not essentially a cellular phenomenon at all, but as a series of events affecting the whole protoplasmic mass of the egg and the embryo. Development is then primarily an activity or function of the organism as a whole, and this is manifest even at the very beginning when the organism is monoenergid. Cell-division and even nuclear division are, strictly speaking, secondary phenomena, and do not in the early stages of development bring about differentiation, though they may facilitate the course of differentiation and consolidate its progress. The main function of nuclear division during segmentation is to break up the substance of the large inert egg-nucleus and distribute throughout the substance of the egg numerous smaller and more active energid-centres. The nucleus has nothing more and nothing less to do with development and differentiation than it has to do with the other physiological activities of the organism. Being essential for constructive metabolism and the maintenance of life, it is necessarily associated intimately with the processes of development, which could not take place without it. The presence and activity of nuclear substance is then a primary condition of embryonic development, as it is a primary condition of life at all. As Brachet says, with regard to the nucleus,

‘It is, in the egg as elsewhere, an essential element of cellular life. If the egg is a cell, it is because it has a nucleus. The nucleus participates in the activity of which the egg is the seat, an activity which after long detours results in the formation of a new organism, and from which nuclear action cannot be excluded; but we do not know in what exactly this action consists, nor exactly what role the nucleus plays in the functioning of any cell’ (p. 304).

7. In conclusion, a few remarks upon the relation between growth, differentiation, and cell-division in plants may not be without interest, as reinforcing our contention that differentiation is essentially an activity of the organism rather than a composite function of its cellular constituents.

Rauber remarked in 1883 that while most zoologists of his day, following Schwann and Virchow, accepted the elementalist conception of the living thing, and considered differentiation to be the result of cell-activities, the botanists — particularly Hofmeister, Sachs, De Bary, and Goebel — took the opposite view that growth and differentiation were functions of the organism as a whole and cell-division a result rather than a cause of these activities. Rauber himself was on the botanists’ side; he pointed out that it is more rational to consider growth as the cause of cell-division rather than the other way about (p. 252). Sachs devotes much attention to this important question in his lectures on plant physiology.

1 He regards as ‘utterly mistaken’ the view that growth and differentiation can be ascribed to the activities of individual cells.

‘Growth — i.e. the increase in volume and change of form — may take place in plants even without accompanying cell-divisions. In this connection I have already repeatedly referred to the non-cellular plants, such as Botrydium , Caulerpa , Vaucheria> etc., and particularly to the Myxomycetes. It is important to bear this fact in mind; because it proves that the formation of cells is a phenomenon subordinate to, and independent of, growth. The excessive importance for organic life hitherto ascribed to cell-formation found expression in this direction also, in that it was believed that growth depended upon the formation of cells. This is, however, not the case. On the other hand, however, the fact is of course important, that while a few hundred simple forms of plants exist in which growth is not accompanied by cell-division, in all other plants growth and cell-division are intimately connected with one another. In attempting, then, to make clear the relations of the two processes — growth and cell-division — it is above all to be insisted upon that growth is the primary, and celldivision the secondary and independent phenomenon’ (p. 431).

It should be noted that Sachs uses the word ‘growth’ to include differentiation. He regards cell-division as merely a diminution in the size of the chambers into which the livingplant substance is divided, consequent upon growth and conditioned by growth (p. 95). The general plan of growth is determined by the ‘growing point’ as a whole; what is formed is then secondarily divided up into cells. In the growing shoot of the sea-weed Styfocaulon , for example, the shape of the branches and the method of branching appear first, and cell-division sets in only when growth has been completed. We have, in this case, at the upper end of shoot growth without cell-division, and in the older portions of the shoot cell-division without growth (p. 435).

1 J. von Sachs, Lectures an the Physiology qf Plants , Eng. Trans., Oxford, 1887.

Both in cellular and in non-cellular plants the nuclei are most numerous and most closely crowded together at the growing points, from which differentiation sets out; Sachs interprets this phenomenon physiologically, in terms of his energid theory — multiplication of nuclei at these points is necessary to supply the metabolic energy for growth; partitioning off of the energids is a secondary and derivative process.

   The interpretation of development and heredity (1930): 1 Introductory | 2 Aristotle’s ‘De Generatione Animalium’ | 3 Preformation and Epigenesis | 4 The Germ-Plasm Theory | 5 The Theory of the Gene | 6 Some Modern Epigenetic Theories | 7 Wilhelm Roux and the Mechanics of Development | 8 The Mnemic Theories | 9 Retrospect. The Use and Misuse of Abstraction | 10 The Organismal Point of View | 11 The Physiological Interpretation of the Cell Theory | 12 The Cell and the Organism | 13 The Cell in Relation to Development and Differentiation | 14 The Organism as a Whole in Development and Reproduction
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