Waddington1956 2

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Waddington CH. Principles of Embryology (1956) The MacMillan Co., New York

   Principles of Embryology (1956): Part 1 - 1 The Science of Embryology | 2 The Gametes | 3 Fertilisation | 4 Cleavage | 5 The Echinoderms | 6 Spirally Cleaving Eggs | 7 The Ascidians and Amphioxus | 8 The Insects | 9 The Vertebrates: The Amphibia and Birds | 10 The Epigenetics of the Embryonic Axis | 11 Embryo Formation in Other Groups of Vertebrates | 12 Organ Development in Vertebrates | 13 Growth | 14 Regeneration | 15 The Role of Genes in the Epigenetic System | 16 The Activation of Genes by the Cytoplasm | 17 The Synthesis of New Substances | 18 Plasmagenes | 19 The Differentiating System | 20 Individuation - The Formation of Pattern and Shape | References
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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Chapter II The Gametes

Development in sexually reproducing organisms is usually considered to begin at the time when the sperm unites with the egg. But actually these two types of cells are among the most complex formed in the animal body, and themselves undergo very important processes of development before they are ready to perform their characteristic functions. The undifferentiated cells which will eventually give rise to them are collectively known as gametocytes, and separately as oocytes if they will form ova, or spermatocytes if they will form sperm. The fully differentiated cells are known as gametes. The male type are called sperm, or spermatozoa, both terms being correct and with exactly the same meaning. The female type are referred to as eggs or ova, but these two words do not mean quite the same thing. The word ovum refers strictly to the gamete-cell; and this often makes up only a part of the body known as the egg, which may include a number of membranes, layers of jelly, shell, etc., which strictly speaking lie outside the ovum, and are no part of it. Thus in the hen’s egg, the ovum is only that part conventionally known as the ‘yolk’.


The basic functions of the gametes are, firstly, to bring together the two nuclei contributed to the offspring by the parents, and secondly to carry out the development of the new individual until it is fully enough formed to take in its own nourishment. A good deal of preparatory differentiation is required before an ordinary cell can be fitted for either task. It is not appropriate here to discuss in any detail the preparation of the gamete-nucleus, since this subject really belongs to the allied discipline of Genetics, and is fully described in textbooks of that subject. It is only necessary to remember that, whereas the nucleus of a normal body cell contains two of cach kind of chromosome, and thus two of each kind of gene, in the gamete-nucleus these are reduced to one representative of each kind. The reduction takes place by a sequence of two divisions, known as the meiotic, or maturation divisions (the term ‘reduction division’ cannot strictly be applied to either the first or second of these, but only to both together). The matured gamete-nuclei, containing only one of each sort of chromosome, are known as haploid, while the normal condition is known as diploid.


  • 1 In some organisms (many plants and a few animals) the body cells contain more than two of each kind of chromosome, and are then said to be ‘polyploid’; in this case the gametes, if they are formed at all regularly, contain half the number in the body cells, and thus more than the haploid number; but many irregularities occur in such cases.

1. Spermatogenesis

In the development of sperm, the two meiotic divisions occur fairly early in the history of the spermatocyte, usually with only a short interval between them. Since there are two maturation divisions, and each division gives rise to two similar daughter cells, one spermatocyte which starts the process will eventually form four sperm. Usually they separate from one another, but in some species they remain together as a group (Fig. 2.1).


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Figure 2.1 Diagram of the formation of sperm (on left) and eggs (on right).


At the time when the maturation divisions occur, the spermatocytes are fairly normal-looking cells; the main differentiation by which they become transformed into sperm occurs in the haploid daughter cells. In a few groups, the fully differentiated sperm are amoeboid (e.g. some Crustacea), but in most animals they are built on roughly the same plan, consisting of three main parts; a head containing the nucleus, a middlepiece containing one or more centrosomes, and a flagellar tail which serves as an organ of motion. (For a comparative account of sperm morphology, see Retzius 1902-1909.) The processes of formation of these specialised parts of the cells have been the object of considerable microscopial study (cf. Gresson 1948) but the results have not been very clear cut, nor have different investigators always reached agreement. This is nowadays not so surprising, since studies with the electron microscope have shown that sperm contain many structures which are well below the resolving power of the light microscope, so that studies with the latter could not be expected to reveal the mode of their formation. The electron microscope work is still in its infancy, and again it is the case that agreement on the structures has not yet been reached. What is important is that this new tool has shown that the material architecture of the sperm is certainly very much more complicated than had been suspected. An indication of the degree of complexity involved may be had from Fig. 2.2, which shows the structure of the middle piece of a ram’s sperm, as interpreted by Randall and Friedlaender (1950). Even if some revision later turns out to be necessary to this picture, it is impressive to discover that such an apparently simple object can contain so many structurally distinct components arranged in such definite and elaborate patterns.


The spermatozoon is a small light cell, capable of independent movement. It plays the active role in fertilisation, in contrast to the immobile and passive egg. This activity is, in fact, the basic definition of a male gamete; in some organisms the sperm is very unlike the common pattern just described, and in lower plants, for instance, there may be very little difference in shape between the female and male gametes; but wherever there is a difference in activity, we say that the more active type is the male, the less active the female. Whether there is any more fundamental similarity, other than their activity, between the male gamete of an Alga and a mammalian spermatozoa, remains rather a debatable question.


The metabolism of sperm is being very actively studied at the present time, both for its own intrinsic interest, and on account of its importance for the technique of artificial insemination. Reviews of recent work on mammalian semen and sea-urchin sperm will be found in Mann (1949, 1954) and Rothschild (19514).

2. Oogenesis

The formation of the egg-cell is a more complicated and more lengthy process than the formation of the sperm. As a bearer of a haploid nucleus, the ovum has a somewhat simpler task than the sperm, since it does not need to produce any means of locomotion. But this simplification is more than outweighed by the fact that it is out of the cytoplasm of the ovum that the main structures of the embryo must be formed. The egg must in the first place contain sufficient reserves of nutriment to keep the young animal alive till it can obtain its own food, and although some of these stores can, as we have mentioned, be provided outside the egg-cell proper, yet in most cases such an expedient is only resorted to after the ovum itself has been loaded to capacity. Further, apart from reserves of food, the egg cytoplasm must embody in some way the structural basis out of which the embryonic body can be formed; and this, one can see, must involve an elaborate process of preparation. It is not surprising, therefore, that the comparatively simple maturation of the sperm is profoundly modified in the differentiation of eggs (Fig. 2.1).


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Figure 2.2 Structure of a typical mammalian spermatozoon (that of the ram). On the left a light microscope picture of a complete sperm, on the right an interpre tation of the structure of the middle piece as revealed in the electron micro~ scope. (From Randall and Friedlaender 1950.)


The essential feature of the modification is the intercalation of a long stage of growth into the sequence. This occurs, in oocytes, before the first maturation division is completed; usually, in fact, the first division starts, and then goes as it were into a state of suspended animation while the cytoplasm and even the nucleus enlarge to many times their original volume. In some eggs (most invertebrates), the maturation divisions are not resumed until stimulated to do so by fertilisation. In others, such as most vertebrates, the egg completes its first division, but sticks again in the middle of the second until fertilised; it is only in a few types (c.g. echinoderms) that both the maturation divisions are completed before the eggs are shed from the ovary.


The intercalated growth stage not only interrupts the continuity ofthe maturation divisions, but also modifies the relation between the division of the nucleus and the cytoplasm. It is as if the production of one full-sized egg were as much as one oocyte can manage; if, in the middle of its process of growth, each oocyte were to divide into two and then again into four equal parts, it would have to produce enough substance to make four eggs. The necessity for such an enormous achievement is avoided by making the cytoplasmic divisions extremely asymmetrical, only a tiny lump of cytoplasm being cut off from the main body of the egg, which remains substantially intact. The first of the lumps is formed, in marine eggs, at the end of the egg which floats uppermost. This end is known as the ‘animal pole’ (the opposite, heavier end being the ‘vegetative pole’). The small cell produced by the first maturation division is thus known as the first ‘polar body’. In the second maturation division it may divide again, while a second similar small body is given off from the egg. Thus the maturation divisions, instead of producing four ova from one oocyte, finally give rise to one ovum and three polar bodies. The latter soon degenerate, and, except in very peculiar circumstances, play no part in the development of the embryo. During the growth of the oocyte, there is considerable activity both in the nucleus and in the cytoplasm. The former enlarges greatly, becoming a so-called ‘germinal vesicle’, filled with a voluminous nuclear sap. It is one of the great gaps in our knowledge of oogenesis that we know so little about the constitution of this sap, except that it is rich in sulphydrylcontaining proteins (Brachet 19524; Brown, Callan and Leaf 1950). The chromosomes, arrested at some stage in meiotic prophase, usually tend to enlarge and become less densely staining. In highly yolky eggs which have a long growing period, this expansion of the chromosomes proceeds very far, with the production of peculiar so-called ‘lampbrush’ forms in which the basic chromosome threads (the chromonemata) are clothed in a fluffy mass of thin hair-like projections (Fig. 2.3). Chromosomes at this stage stain very weakly in many of the dyes for which more normal ones show great affinity, and in particular they are difficult to stain in the Feulgen reagent which is more or less specific for desoxyribose-nucleic acid; nevertheless it appears that they never entirely lose their stainability in this dye, and it is probable that desoxyribose-nucleic acid, which in all other circumstances appears to be an essential constituent of chromosomes, is present on them throughout oogenesis also (Callan 1952).


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Figure 2.3 Structure of the loops of ‘lampbrush’ chromosomes from the germinal vesicle of the newt odcyte. The chromonema runs horizontally across the drawing. It bears small swellings (chromomeres) which are double. From these arise loops, which are usually symmetrical about the axis of the chromonema, but asymmetrical along the length of the chromonema. (From Callan, unpublished.)


Accompanying the expansion of the chromosomes, there is also an enlargement of the nucleolus, which often throws off smaller bodies so that the nucleus comes to contain many nucleoli (Fig. 2.4). The chemical constitution of these is different from that of the chromosomes; they contain much ribose-nucleic acid but no desoxyribose, and also much protein of a basic type involving arginine. Substances of the same general kind as those present in the nucleoli can be found in the cytoplasm, particularly in the immediate neighbourhood of the nuclear membrane, and it has been suggested that the nucleoli are important sites for the synthesis of basic protein-nucleates, which pass through the nuclear membrane and later control the synthesis of further cytoplasmic proteins (p. 382). The extrusion of quite large droplets of nucleolar material into the cytoplasm can be clearly seen in some forms (Fig. 2.5, p. 38). It is probable, indeed, that ribose-nucleic acid compounds are some of the most important constituents in the cytoplasm of the growing oocyte, since they seem to be involved in the protein synthesis which must be taking place very actively there. During the growth of the oocyte they increase in amount, but not as fast as the total volume of the cell (Osawa and Hayashi 1953). Caspersson and Schultz (1938) claimed that in Drosophila the quantity of such nucleotides in the oocyte was increased in eggs formed in mothers which have extra heterochromatin (in the form of a supernumerary Y chromosome) but this has been disputed by Callan (1948), and it is not clear what relation exists, if any, between the cytoplasmic and nucleolar ribonucleic acid on the one hand and the heterochromatic parts of the chromosomes on the other.


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Figure 2.4 An early and a middle stage in the development of the germinal vesicle in the odcyte of the snail Helix aspersa. The nucleus contains a large nucleolus, and by the later stage shown there are many small nucleoli in addition. The dotted region in the cytoplasm is the ‘yolk nucleus’. (From Serra and Lopes 1945.)


In spite of the ribonucleic acid materials apparently given off from the nucleus, it is probable that the latter is not the main site of synthesis in the oocyte. In fact, Brachet (19526) has argued that the nucleus contains less than its due share of the cellular enzymes, and, for instance, accounts for only a very small fraction of the respiration of the cell; this result, however, was probably a consequence of inadequate methods of cultivating the isolated amphibian germinal vesicle with which he worked, and as far as respiration is concerned, the nucleus is probably just as active as the cytoplasm (Callan 1952).


It is in the latter, however, that the major synthesis of the food reserves takes place. In many organisms there appears in the cytoplasm of the young oocyte a body which has received the name of the ‘yolk nucleus’. It is particularly well seen in the eggs of some spiders, in which it has a laminated structure and is birefringent. In Amphibia it is represented in the young oocyte by a small mass in the cytoplasm which later expands and disperses to form a peripheral sheet lying just below the outer surface of the cell. It is usually considered to be constituted of mitochondria, and histochemical tests reveal the presence in it of fats, including the peculiar phosphatides which give the so-called plasmal reaction, and of several enzymes such as indophenoloxidase, dipeptidase, etc. It appears almost certain that the yolk nucleus is the seat of a particularly active synthesis of fats and proteins.


The reserve foodstuffs in eggs are often collectively referred to as ‘yolk’. But this is really a loose use of the word. Strictly speaking, the true yolk is only one part of the reserve; it consists of platelets or lumps of a proteinlipoid substance. Besides it, the reserve contains globules of more or less liquid fat, and granules of carbohydrate, which are usually in the form of glycogen. In ova which contain fairly smal] quantities of reserves, these materials may be scattered more or less evenly throughout the cytoplasm; such eggs are known as ‘oligolecithal’, meaning that they contain little yolk. In most eggs with more than a very small quantity of reserve material, this is accumulated towards one end, the heavy vegetal pole referred to above; such eggs are called ‘telolecithal’. There is a whole range of them, from only moderately yolky forms to bird or teleost eggs, in which the enormous mass of reserve food almost swamps the tiny patch of living cytoplasm. As a very rough general rule, the more highly evolved animals have more yolky eggs. Thus many marine invertebrates have rather little reserve, since their embryos can at a very early stage obtain nutriment from the microscopic living creatures of the sea. Vertebrates, in which the embryo cannot feed itself until it has developed a mouth and a gut, have much more yolk; even the amphibian egg is packed with yolk platelets, most fish have still more, and reptiles and birds most of all, as well as extra-ovular reserves in the form of the ‘white’. But the rule breaks down for mammals, in which the embryo is fed through the maternal placenta; although the monotremes, the most primitive representatives of the mammal stock, have eggs nearly as yolky as reptiles, in the true mammals the ovum contains scarcely any reserve. Most insect eggs, on the other hand, have a great deal of yolk, which is accumulated towards the middle instead of at one end (these are spoken of as centrolecithal eggs).

3. Follicles and membranes

During growth within the ovary, the cortex of the egg is usually closely invested by a layer of so-called ‘follicle cells’ which, presumably, play a major part in transmitting the materials for the growing oocyte; they may also be the main determinants of the cortical structure, although this is not definitely known. In mammals, the layer of follicle cells becomes very thick; in fact they increase to a largish spherical mass, within which a secretion is formed which hollows out the mass until the oocyte is hanging from a sort of stalk. This secretion contains the ‘follicular hormone’ which produces oestrus in the female mammal. When the egg is ripe, the follicle bursts and the egg, still surrounded by a layer of follicle cells, is set free to reach the Fallopian tubes and thus travel down to the uterus; meanwhile the remains of the follicle forms the “yellow body’ or corpus luteum, from which is secreted the luteal hormone, an important factor in pregnancy.


In other animals, the follicle cells are less in evidence, although probably always present. In insects the eggs are arranged in strings in the ovary; and there may be no special nutritive cells, or a group between each egg, or a single group at the end of each string with projecting strands leading down to the growing eggs (Fig. 2.5). The follicle cells or ‘nurse’ cells, as they are also called, are themselves often the site of active synthesis. In Drosophila and other insects their nuclei are polyploid, the chromosomes having divided frequently without any accompanying division of the cytoplasm (Painter and Reindorp 1939); this phenomenon is often found in secretory or synthetic cells in insects. In most cases the substances formed in the nurse-cells are passed almost completely into the oocyte, so that the nurse-cells have almost withered away by the time the oocyte is fully grown.


The processes of oogenesis often include the production of special protective membranes to clothe the egg-cell, though a few types of marine eggs are shed completely naked. Egg membranes are of three kinds; those which are strictly part of the ovum itself, being secreted by its outer surface; those which are formed by follicle cells; and those which may be laid down by the oviduct during the passage of the egg away from the ovary. The first kind are usually known as the vitelline membrane, the second as the chorion, while the third may have a variety of names such as ege capsule, or shell. Vitelline membranes are of very general occurrence, except in the few naked types of eggs. Chorions are not found quite so often; the insect egg provides a good example of them. The tertiary membranes are particularly well developed in many vertebrates (e.g. the shell and albumen of the bird’s egg) but occur also in many other classes (c.g. the egg capsules of molluscs). In some animals, the membranes may be formed before fertilisation, and it is then common to find that a special opening (known as the micropyle) is provided, which allows for the passage of the spermatozoon.


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Figure 2.5 Figures a, b, c show various types of ‘egg-strings’ from the ovaries of insects. In a the eggs are in simple follicles (e.g. Orthoptera); in b the follicles are accompanied by nests of larger ‘nurse cells’ (e.g. Coleoptera, Drosophila); in c there is a larger group of nutritive cells at the end of the string, with channels leading to each egg (e.g. Hemiptera). (After Korschelt and Heider.) Figure d shows the discharge of material from the nucleolus of the germinal vesicle into the odcyte cytoplasm in Limnea. (From Bretschneider and Raven 1951.)


The evolution of suitable egg membranes, and of eggs able to develop inside membranes, was one of the most crucial steps which had to be taken by animals in the colonisation of dry land (cf. Needham, 1931). All animals provide enough organic food reserves to keep their embryos alive until they can feed for themselves, but marine invertebrate eggs do not contain enough of either water or salts; these are absorbed by the embryo from the sea. The necessity for such salts has probably been a handicap to invertebrates in the colonisation of freshwater, and explains the relative poverty of freshwater as compared with marine invertebrate faunas. Fish go one better and provide all the salts their embryos will need, but they also do not cater for the water requirements. The same is true of most Amphibia, though in a few enough water is present in the egg to make possible a very much speeded-up development in a damp spot (e.g. the tree-frog Hyla). By this stage in evolution, eggs had become quite large, so as to contain enough organic matter for the development of an embryo which becomes rather complicated before being able to feed. The reptiles began the next stage, that of enclosing the egg in a shell which could include and retain suffcient water to last till feeding can start. In many of the turtles, the process is incomplete, and some moisture has to be absorbed from the wet sand in which the eggs are deposited. In birds the problem has been fully solved; and in mammals it is, of course, circumvented by the device of uterine development. It is interesting to note that water birds, instead of taking advantage of their environment to relax the effort to retain water in the egg, still provide sufficient stores for the developing embryo, and even evolve a waterproof shell to prevent more water entering. This is an example of a rather general rule of evolution, often known as Dollo’s law, which states that evolutionary changes are irreversible. If a later animal returns to a set of circumstances similar to those in which one of its remote ancestors lived, it nearly always meets them, not by an exact return to the ancestral adaptation, but by some new expedient.


The evolution of an egg-shell which would retain water solved one of the problems of land life only to raise others. The shell which encloses the water also keeps in the nitrogenous waste products of embryonic metabolism. It is a rather general rule that during the earliest stages of embryonic life the main reserve foodstuff utilised is carbohydrate (glycogen); next comes a stage when the protein is consumed, and last of all the fat (but see p. 454). It is the second of these, in particular, which gives rise to large amounts of nitrogenous waste. Animals with shelled eggs cannot avoid using such materials altogether, although they contrive to become very efficient in converting yolk protein into body protein without producing much waste; and they manage also to start rather early to consume fat, which has the added advantage that it produces some extra water as a final product of its oxidation. But even so, there is a good deal of nitrogenous waste to get rid of. In the simplest marine forms, this is excreted as ammonia, a highly poisonous but rapidly diffusible substance. In fish, more efficient excretory organs are produced, and the waste products are got rid of in the less poisonous, but less diffusible form of urea. It is characteristic of land animals, that most of their nitrogenous waste is excreted as uric acid, which is a very insoluble substance. The reason why this mechanism has been evolved is almost certainly in order to cope with the situation of the embryo within its water-retaining shell; being unable to get rid of its waste products it needs to deposit them in a form which will stay put. Thus the exigencies of ovular life have a lasting effect on the metabolism of the higher vertebrates, though mammals, which escape the closed box of an egg-shell, have returned to urea as their main excretory end-product (a fact which does not fit very well with Dollo’s law mentioned above).


It is worth remarking that in animals which eventually excrete uric acid, we find that there are short early stages which excrete ammonia, like the carliest ancestors, and urea, like the rather more recent ones (Needham 1931, 1942). This is a biochemical example of the phenomenon of ‘recapitulation’, which we have discussed as it applies to morphological events (p. 9).

4. The morphogenetic structure of the egg

The nutritive materials in the ovum are more or less ‘inert’ in that they play little part in determining the structure of the developing embryo. As we have seen, the yolk usually occupies a definite position within the egg-cell, but it can be shifted about, for instance by centrifuging the egg, without making any great difference to the course of development. The underlying basis of the embryonic body is to be found rather in the nonyolky cytoplasm. This is often optically clear and fairly homogeneous, and is therefore rather difficult to investigate. Many eggs contain, besides food reserves, a number of other granules, which may be grains of pigment, or mitochondria at which enzyme activity occurs, or may be of a so-far-undetermined nature (Fig. 2.6). We shall have to describe later eggs in which different regions of cytoplasm can be recognised by the different types of granule which they normally contain (e.g. in ascidians p. 106). But again, at least in many cases, the larger granules do not themselves determine the development of the different regions, since, like the yolk, they can be shifted by centrifuging without affecting it. On the other hand, we shall find examples (again for instance in ascidians) where, if the centrifuging moves the actual clear ground substance of the cytoplasm, together with the ultra-microscopic granules, the ensuing development is profoundly altered. In such cases, it is clear that the different parts of the egg cytoplasm are endowed with different developmental properties.


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Figure 2.6 The internal constituents of the odcyte of the snail Limnea, as seen after centrifugation. On the right the distribution of the various components is shown diagrammatically, on the left is a drawing of an actual section. (After Raven 1948, and Bretschneider and Raven 1951.)


In other eggs, such as those of echinoderms, one can move even the internal cytoplasm around a good deal without interfering with development. But even in such cases, there are probably always some structures in the egg whose integrity is essential for the formation of a normal embryo. The most frequent location of this essential structure is the surface layer. The cytoplasm here is generally stiffer and more elastic than it is within the egg-cell, forming an external layer known as the ectoplasm or cortex. It may be entirely clear, or it may contain a special layer of granules; and it may have a definite external pellicle or vitelline membrane—in any case, we shall see that a new membrane frequently forms from it at fertilisation. The cortex is so stiff that it is difficult to move by centrifuging, and, in eggs where normal development occurs after rearrangement of the interior, it seems that the reason is that the essential normal structure is still retained by this elastic external layer. We know very little about the nature of this essential structure. It is often spoken of as a ‘gradient’; but this means little more than that the animal end of the egg differs from the vegetative and that there is a gradual transition between them. Probably the essential properties of the different regions depend on sub-microscopic structures in the protein framework of the cortical cytoplasm; but if this is so, we shall have to await the development of new techniques of investigation before we can learn much about them (Fig. 2.7).


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Figure 2.7 Three fundamentally different types of egg structure. On the left, a ‘mosaic’ egg with localised regions of cytoplasm (the oligochaete, Tubifex, after Penners). Centre, the echinoderm egg, with a general polarity, indicated by the dark and light circles, and two opposing gradients, shown by the plus and minus signs (after Harrison), Right, an amphibian egg, with a vegeta~ tive-animal gradient dependent on yolk concentration, and a cortical gradient falling off from the position of the future blastopore. (After Dalcq and Pasteels.)


In spite of the fact that our knowledge of these structural properties of the egg-cell is so slender, one must not overlook their fundamental importance. When we discuss the eggs of the different kinds of animals, we shall in every case find that the eventual origin from which the whole later development springs is the orderly arrangement of essential parts of the ovum. We must therefore enquire a little more deeply how this arrangement is brought about. In particular, what is the relation between it and the hereditary factors or genes which determine the detailed character of the adult organism? It was for a long time argued by many biologists that genes affect only minor and trivial processes in the latter stages of development, while the major outlines of the animal body are determined not by them, but by the nature and structure of the egg cytoplasm. This theory made no suggestion as to what determined the nature of the egg in its turn, and was therefore always somewhat incomplete. But this was not its worst fault; in the only suitable cases which have been properly investigated, we have evidence that the theory is incorrect.


There are not many examples of animals in which there are two or more variants in the basic structure of the egg cytoplasm, but a few cases are known. For instance, the eggs of molluscs cleave with a spiral pattern (p. 60); and this spiral may be either right- or left-handed, a few species having variants of the two kinds. In the pond-snail Litmnea, the inheritance of such variations was studied by Boycott and Diver (1923, 1930). The right-handedness or left-handedness of an egg depended in a straightforward way on the genes in the mother in whose ovary it was formed. This is a clear case of a difference in egg cytoplasm, which is inherited by means of genes, exactly as are differences, for instance, in the formation of pigment in an eye-cell. The only slightly odd feature of the situation is that, whereas one normally looks for pigment within the cell in question, we find it more convenient to diagnose the nature of Litmnea egg cytoplasm by waiting to see which way the fertilised egg will cleave; but that is a mere matter of the technique of study. The important point is that in this case we can prove that the fundamental outline of the embryonic organism is based on the egg cytoplasm, but that this in its turn is determined by genes, just as any other character is (Fig. 2.8). It is still quite uncertain how these genes operate. One possibility is that they influence some asymmetry which might exist in the protein molecules of the egg cytoplasm; but this is rendered unlikely, though not perhaps impossible, by the fact that the structure of the sperm, which are also spiralised, is not affected by the genes which control the symmetry of the eggs (Selman and Waddington 1952).


Other examples of the control of the egg cytoplasm by the genes in the maternal ovary are provided by the ‘female-steriles’ in Drosophila (p. 135).


We may almost certainly conclude that in all eggs the basic structure of the cytoplasm is laid down in the maternal ovary while the ovum is being formed, and that it is as fully dependent on the genes of the mother as is the character of her eyes or skin or hair. If this is so, we should expect to find a regular relationship between the main structure of the egg and the position in which it lies in the ovary. This question has not had as much attention in recent times as it deserves. It is known that in many insects with elongated, banana-shaped eggs, the long axis of the egg always lies along the long axis of the insect; in some invertebrates, the position of the egg nucleus and of the accumulation of yolk has a definite relation to the blood supply, and the same has been claimed to be true of frogs’ eggs. But in most of the types of eggs in which the internal structure is clearest (e.g. ascidians) we know very little about the geometry of their formation within the ovary.


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Figure 2.8 The 4-cell stage and the adult shell of dextral (1, 2) and sinistral (3, 4) Limnea peregra. (After Robertson 19 53-) (5) Shows part of the tail of Limnea sperm, consisting of three large and one small strand wound, always in a dextral spiral, round a central core. (After Selman and Waddington 1952.)

Suggested Reading

Rothschild 1951.



   Principles of Embryology (1956): Part 1 - 1 The Science of Embryology | 2 The Gametes | 3 Fertilisation | 4 Cleavage | 5 The Echinoderms | 6 Spirally Cleaving Eggs | 7 The Ascidians and Amphioxus | 8 The Insects | 9 The Vertebrates: The Amphibia and Birds | 10 The Epigenetics of the Embryonic Axis | 11 Embryo Formation in Other Groups of Vertebrates | 12 Organ Development in Vertebrates | 13 Growth | 14 Regeneration | 15 The Role of Genes in the Epigenetic System | 16 The Activation of Genes by the Cytoplasm | 17 The Synthesis of New Substances | 18 Plasmagenes | 19 The Differentiating System | 20 Individuation - The Formation of Pattern and Shape | References
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Cite this page: Hill, M.A. (2020, October 26) Embryology Waddington1956 2. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Waddington1956_2

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© Dr Mark Hill 2020, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G