A textbook of general embryology (1913) 4
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Kellicott WE. A Textbook of General Embryology (1913) Henry Holt and Co., New York.
Kellicott (1913): 1 Ontogeny | 2 The cell and cell division | 3 The germ cells and their formation | 4 Maturation | 5 Fertilization | 6 Cleavage | 7 The germ cells and the processes of differentiation, heredity, and sex determination | 8 The blastxtla, gastrula, and germ layers. Morphogenetic processes
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Chapter IV. Maturation
In this chapter we shall describe certain events which are in reality essential steps in the processes of oogenesis and spermatogenesis, namely, the maturing of the nuclei of the definitive germ cells. In animals these maturation processes are the final steps in the complete specialization of the germ cells, and must be accomplished before the two gametes can fuse completely and thus begin the life of the "new" organism as an individual. As a matter of fact, the processes of maturation may be inaugurated before the growth and differentiation of the germ cells are entirely completed, and these processes may then all go on together. They are considered here separately, and without complete regard for their normal time relations, partly as a matter of convenience, looking toward simplicity of description, and partly to emphasize their great importance as a period in the development of the organism. Such a separation is easy because the maturation processes are not visibly connected with the genesis of the germ cells as such, for, morphologically at any rate, they concern only or chiefly the nuclei alone; the accompanying cytoplasmic modifications of structure have already been described.
That morphological characteristic chiefly distinguishing the fully matured germ cells is the possession of but one-half the number of chromosomes, and of but a smaller fraction of the amount of chromatic material, possessed by the somatic cells (Van Beneden) . We should include under the term maturation, the whole series of events leading to this reduction in number of chromosomes and amount of chromatin. It should be noted, however, that the terms " oogenesis and " spermatogenesis have sometimes been used in a restricted sense to mean what we here term "maturation," but we have understood the former terms to include the whole history of the germ cells up to the time of their formation as completely specialized structures, and maturation therefore becomes a phase in oo- and spermatogenesis.
It is a familiar fact that in fertilization the union of an egg nucleus and a sperm nucleus is an essential step. The repeated union of nuclei of the usual type, in this way, would result in rapid and limitless increase in chromatic elements and material, but for the operation of some mechanism preventing such an accumulation, and yet permitting the fusion of germ-cell nuclei. Maturation is such a process; but it is much more than this. Consideration of all the phenomena of maturation raises many questions, important, even fundamental, in their biological significance. The full meaning of the phenomena can be appreciated only in connection with the fertilization processes to which they are introductory; we may most profitably, therefore, postpone much of our discussion of the general significance of maturation until we have become acquainted with the process of fertilization.
At this time, then, we shall describe the essential facts of maturation as we find them in typical, in some respects perhaps schematized, form, together with a brief comparative account of some maturation processes in a few special instances. Then after a similar account of fertilization in the next chapter, we shall be in position to consider some of the general aspects of both these processes taken together. The events of maturation and fertilization are really closely related in time, as well as in significance. While the spermatozoa are always fully mature before they enter the egg cells, the entrance of the sperm may occur either before, during, or after the maturation of the ovum, although of course the essential step in fertilization, namely, the union of the nuclei, does not occur (excepting in some Protozoa and plants) until after the maturation of the egg nucleus is completed.
The maturation of the germ cells is accomplished, in the Metazoa, by a modification of a mechanism common to all cells and already familiar, namely, mitosis. But the cell divisions which occur here are of a very special form, not found in the history of other kinds of cells. These unusual mitoses are known as the meiotic {maiotic, Farmer and Moore), or reducing divisions, and their chief peculiarity consists in the fact that they result in the formation of daughter nuclei containing the reduced or haphid number of chromosomes.
We shall review first the maturation of the spermatozoon, as this is less modified than the ovum, from those conditions which we regard as typical. Throughout the multiplication divisions of the spermatogonia, the mitoses are all of the usual character, except that the mitotic figures are relatively larger than in the somatic divisions. The number of the chromosomes is the same as in the somatic cells of the same organism; this is spoken of as the diploid number. In many, perhaps most, organisms the chromosomes differ from those of the somatic cells in form and size characters, so that the germinal tissue can usually be identified; the germinal tissue nuclei are in general larger and richer in chromatin than those of somatic tissues, a difference which, as previously noted, in a few forms {Ascaris, Cyclops, some Teleosts) can be traced from very early cleavage stages. But the constitution of the nuclei which pass into the interkinesis after the last spermatogonial division, i.e., into the primary spermatocyte nucleus, is essentially normal. Sometimes certain peculiarities become noticeable during the growth period of these cells; the nucleus frequently does not remain in the typical "resting" condition, but forms a more or less distinct spireme (leptonema, Winiwarter), and sometimes, even at the beginning of this stage, there may be a fission of the chromatin granules, forming a sort of double spireme (Fig. 73). At the close of this growth period, when the primary spermatocyte prepares to divide, the nucleus begins to show a very unusual condition. The nucleus itself remains large, but the chromatin, as it begins to form a spireme, in those cases where this has not formed previously, condenses at one side of the nucleus, in the vicinity of the nucleolus, usually in the region near the centrosomes and perhaps through their influence (Schonf eld), into a dense mass in which little structure can be made out (Figs. 72, 73). This stage is called the contraction phase J or synizesis (McClung) (pachynema, Winiwarter). In some cases synizesis may occur near the beginning of the growth period, throughout which the nucleus then remains in this condition.
Fig. 72. — Early stBgea in the matiuatioii of the Dipnoan, Lepidoeii After Agar, x 933. A. Polar view of equatorial plate of late BpermatoEOiiium, Hhowing size and form differentiation and paitiug of chromosomee. B. Spirema Btage (leptonema) of primary spermatocyte. Only a few of the threads are shown. C Nearly polar view» showing beginning of longitudinal fusion of chromatin threads; beginning of synapsis (zygonema). D. Nearly polar view of "bouquet stage" (pachynema). The threads are fused and condensed. E. FQlar view showing beginning of contraction (syniEesia) and splitting of the chromosomes (diplonenia). Most of the thicliened threads have split apart except terminally, where they remain fused, forming rings. In some, the
When growth of the spermatocjrte is completed this knot of chromatin begins to disentangle and the spireme again becomes visible. This later spireme is not continuous, however, but is of the segmented type (Fig. 72), and the number of segments, i.e. J of chromosomes, is hut one-half the number of chromosomes that went into the nucleus at the close of the preceding division. As regards the chromatic structures, this is the essential point in the whole maturation process; the number of chromosomes formed in the prophase of the first spermatocyte division is reduced to one-half the somatic number. This numerical reduction of the chromosomes is brought about in most, if not in all cases so far known, by an actual fusion, by twos, of the chromosomes contained in the last spermatogonial nucleus. This fusion of pairs of chromosomes is termed synapsis (Moore, McClung) or syndesis (Hacker) (zygonema, Winiwarter), and the resulting units are thus double or bivalent chromosomes. It seems entirely likely, if not definitely established, that the pairs of chromosomes which come together in synaptic fusion are each composed of one chromosome derived from the male parent, and the corresponding chromosome derived from the female parent, similar in size, and form, and also in function if we assume the fact of chromosomal specificity (Montgomery). These two groups of similar elements came into a single nucleus dming the fertilization process which was the beginning of the new individual, whose cells are now preparing for reproduction; they have remained separate throughout the life of this organism until this event, through all the divisions of the ancestral germ-forming cells (Fig. 80). In a certain sense, therefore, this process of S3niapsis represents the real climax of the whole
splitting is less complete. One ring is cut through showing two free ends. F. Advanced synizesis. G. Chromosomes appearing after synizesis, shortened and thickeneci. The ex-conjugant chromosomes (univalent) have separated and show transverse constrictions, preparatory to the second maturation division.
series of developmental processes, and it is at the same time the starting point of the life cycle of a new organism of another generation.
In a few forms {e.g., some Insects, Lepidosiren, Fig. 72), the double nature of these bivalent chromosomes is distinctly visible and is indicated by a split through the long axis of the chromosome, showing that the pair of univalent elements have fused side by side, a condition known as parasynapsis. In most cases observed (other Insects, Amphibia) the fusion is end to end, a condition known as telosynapsis (Wilson's terms). In many instances, however, the fusion seems to have occurred between the granules composing the chromosomes, so that in the bivalent body there is no visible indication of the duplex nature at this time; this is then only to be inferred from the fact of numerical reduction. It is very important to notice that the time relations between synizesis and synapsis may sometimes be just the reverse of that described above, and the synapsis stage may occur first, so that the numerical reduction of the chromosomes occurs at the close of the last spermatogonial division (some plants, Strasburger, Overton).
Following the period of synapsis the nucleus and cell may proceed at once to divide, or there may ensue another resting period, during which the chromosomes again become indistinct. In either case, when the new mitotic figure forms, always after an unusually long prophase which is characteristic of this division, the reduced (haploid) and bivalent chromosomes often show an unusual condition, in that they may prepare at once, not for a single ensuing division, but for two divisions which are to follow immediately, without an intervening resting period.
From this stage onward in the history of the sperm and egg nuclei, two general types of chromosome behavior are sometimes distinguished, although they are connected by transitional conditions and so are regarded as modifications of a single process. As one extreme condition we find a form of chromosome behavior called tetrad formation^ which we may describe, not because it is a typical method of chromosome reduction, but because the facts of reduction come out more dearly in this form of maturation division (Boveri). In cases of tetrad formation, when the chromosomes appear in the primary spermatocyte, after the resting stage, each of the newly organized bivalent elements comes out in the form of four email bodies, the tetrads, arranged approximately in a square (Fig. 73, E). These bodies result from two successive splittings of each chromosome into four columns of granules, each of which is then condensed into a single element (Fig. 73, A, B, C, D). We may recognize here a precocious division of the chromosomes, which in these cases precedes considerably the division of the nucleus and cell as a whole. Not only this, but there are two chromosomal divisions, corresponding with two cell divisions, and these occur simultaneously, while the nuclear and cytoplasmic divisions occur consecutively at a later period, during which these chromosomes do not divide again. The number of tetrad groups is thus the same as the haploid number of chromosomes l^L and the total number of elements composing the tetrads is four times the haploid or two times the diploid number (2s).
Fig. 73. — Tetrad formation in the spenaatogenesis of Ascari> mfgalocejAala bivaiens. After Brauer. X 795. A-O. Stages in the djviaion of the primary spermatocyte. A, B. splitting, and C, condenaation of chromatin tbread, seen in Bide view. D shows, in end view, that the aplitting is double. CcntroBome divided. E. Migration of centrosomea and formation of spindle. F, Q. Separation of the two groups of dyads and division of the cell body. H. Secondary spermatocyte containing two dyads. I. Division of secondary epermatocyte. /. Two of the spermatids, each with two " monads " or single, univalent, chromo
The nucleus and cell now enter upon a mitosis in which each tetrad behaves as a typical chromosome. The division and migration of the centrosomes to opposite sides of the nucleus, the formation of the spindle and asters, and other details of this mitosis, have no unusual features and need not detain us. The tetrads, containing all told 25 elements, become arranged about the equator of the spindle and each separates into two pairs of elements called the dyads (Fig. 73, F, G). The groups of dyads then move to opposite poles of the spindle and the cell divides into the two secondary spermatocjrtes. Since the resting stage is now omitted, the dyads do not dissolve after this division, nor do they divide again in anticipation of the next mitosis — ^the division of the chromatic elements for this cell division has already occurred in the nucleus of the primary spermatocyte, as we have seen. The dyads, containing all told s elements, then move at once to the equator of the new spindle, and each separates into two monads (Fig. 73, I, J). The two groups of monads, each now containing ^ elements, diverge to opposite poles of the apindle, and the division of the cell (secondary spermatocyte) results in the formation of two sper matids, each with ^ chromosomes (Fig. 74).. Each nucleus then reforms into a typical resting condition, and passes through the metamorphosis into the head of the spermatozoon, as described in the preceding chapter. The essential characteristic, therefore," of the nucleus of the spermatid and spermatozoon is that, while each of the bivalent chromosomes of the spermatocyte is represented, yet, as the result of the process of reduction through synapsis, the chromosomes are now only half as numerous as in all the other cells of the organism. But while each bivalent chromosome is thus represented, it may be a question whether each univalent chromosome is also somehow represented. To this we shall return later.
Fig. 74. — Diagram of reduction with tetrad formation in sperm atogenesTsv. From Wilson, "Cell." The somatic number of chromosomes is supposed to be< four. AtB. Division of one of the spermatogonia, showing the full number (four) of chromosomes. C Primary spermatocyte preparing for division; the chromatin forms two tetrads. D,E,F. First division to form two secondary spermatocytes each of which receives two dyads. G,H, Division of the two secondary spermatocytes to form four spermatids. Each of the latter receives two single chromosomes and a centrosome which persists in the middle-piece of the spermatozodn.
But the formation of tetrads is by no means of universal, even of common, occurrence in reducing divisions. Tetrads arecommonly found only among the Nematodes, Annelids, and Arthropods. In the great majority of animals the reduction divisions proceed without the formation of actual tetrads in their typical form, and when the bivalent chromosomes appear in the nuclei of the primary spermatocytes, as the result of synapsis, they tave no unusual form. As they pass into the equatorial plate, however, it is seen that the two longitudinal halves, coQiposing each bivalent chromosome, are united at their ends (Figs. 72, E;75). When the anaphase begins each chromosome-half is drawn out first from its middle, so that the whole original chromosome may appear as a ring or cross, or some related figure. As the halves separate each may assume a t"- or >-form, the limbs of which may come to lie parallel as the chromosome approaches the pole of the spindle, and thus may appear to be double (Figs. 75, 20). On account of this peculiar form assumed by the chromosomes in this division, it is known as the heterotype division. And it is to be noted that the separation of the halves of the bivalent chromosome here, is along the line of a split which is usually visible in the chromosomes when they appear out of the resting nucleus. As the result of this heterotype division each secondary spermatocyte receives the haploid number of chromosomes. The second mati^ation division commonly shows none of these rings or crosses, or other figures, and is known consequently as the homotype division (Flemming's terms). The homotype division of the secondary spermatocyte follows the heterotype either immediately, or after a considerable pause, during which the chromosomes sometimes lose their definite outlines to some extent. This pause, which does not occur when tetrads are formed, is probably related to the fact that while in the tetrads both divisions of the chromosomes occiu* at the commencement of the process, in this form of reducing division the second splitting does not occur until after its first actual division. During the homotype division the chromosomes behave, then, essentially as in the divisions of the usual type, and the resulting spermatids receive, just as in tetrad formation, the haploid number of chromosomes, just as do the secondary spermatocytes. Numerically, the most important difference in reduction with and without tetrad formation is that in tetrad formation the secondary spermatocytes have the diploid number, and in the absence of tetrads, the haploid number of chromosomes. This is the result of the fact that when tetrads are formed, the division of the chromosomes actually belonging to the secondary spermatocytes (second maturation division) really occurs in the nucleus of the primary spermatocyte (first maturation division), while in the absence of tetrads the division of the chromosomes has the normal relation to cell division, and the haploid number persists from the primary spermatocyte, after synapsis, to the spermatid and spermatozoon.
Fig. 75 — Maturation divisioiu! id certain Insects showiHE forms of chromoBoroes and fheir relation to tetrads After de Sin6ty X 1125. A,B. Two Btages in anaphase of pmnarj spermatooytP division in Stenobolhms parallelus. Rings openin^c into Vs wKk*!! diverge C Anaphase of epfrmatogoniai divisioti in Orphania dfntica-uda showing differentiated ohromoBome x. D, E. Preparation for first spermatocyte diviwon in Orphania, showing "tetrads" in various stages of formation from rings and crosses.
Before mentioning any f\ui;her details of chromosome behavior during maturation, we must compare the process of maturation as it occurs in the oviun with that in the sperm. We may say at the outset that in all essentials the two histories are identical, so that this comparison may be brief, but there are a few differences to be noted*
The divisions of the oogonia are normal ; the diploid number of chromosomes appear, and the details of spindle, aster, and centrosome, call for no special mention. Aside from the chromosomal behavior, the divergences of the later maturation . divisions from the normal are partly the result of the enormous growth of the egg cell, and partly in the nature of adaptation toward ensuring the practically undiminished size of the ovum at the end of the process; that is, an equal subdivision of the chromatic elements is accompanied by an unequal subdivision of the cytoplasm and deutoplasm. The general formation of the large primary oocyte has been described. We should emphasize again the fact that the maturation of this cell frequently is not completed until after the sperm cell has actually entered its substance. If we were describing the events of the maturation of the egg in strict accordance with their usual, though not invariable, time relations we should next describe the ensemination of the egg — the first step in fertilization. For the sake of clearness, however, we shall describe matiffation as if it occurred before the entrance of the sperm; as a matter of fact, there are a few forms in which this is really the normal course of events, as in the sea-urchin and most Echinoderms.
The nucleus of the oogonium is very large and lies toward one side of the cell — practically always toward the animal pole of the egg (Fig. 76,-4). The first steps in the maturation of the ovum closely resemble those in the sperm. During the brief synizesis stage the chromatin condenses near the centrosome, closely around the large "nucleolus" which is commonly found in most oocjrtes; the emerging spireme shows that synapsis has occurred for the spireme is segmented into the haploid number of elements, representing the bivalent chromosomes. That is, the actual reduction occurs in the primary oocyte as in the primary spermatocyte. The oocyte nucleus then passes through a condition not represented in the spermatocyte in that a large amount of chromatin leaves the chromosomes (spireme segments), either dissolving in the nuclear sap, or passing in the form of granules or small masses to some region of the nucleus quite apaxt from the chromosomes proper (Fig. 76). It is important to note that no chromosomes are lost in this way; the full haploid number of these bodies remains grouped at one, usually the distal, side of the nucleus. During the active preparation for the first maturation or heterotype division the nuclear membrane disappears, liberating the dissolved
Fig. 76. — Maturation in the egg of the Nemertean, Cerebratulus, After Coe. C, Z), X 376, others X 260. A. Primary oocyte. Part of the chromatin has been condensed into chromosomes, only five of which are shown (the number present is sixteen). The remainder of the chromatin is thrown out into the cytoplasm. The centrosomes, each with a small aster, are diverging, and the nuclear membrane is commencing to disappear. B. First polar spindle fully formed and rotated into radial position. Chromosomes in equatorial plate. C. First odc3rte division; anaphase. D. First polar body nearly separated. E, First polar body completely cut off; second polar spindle formed and rotating into radial position. Spermatozoon within the egg. F. Second polar body completely separated. Egg pronucleus forming, surrounded by large aster. Sperm pronucleus, also with a large aster, enlarged and approaching the egg pronucleus, c, chromosomes; o, nucleolus, vacuolated and commencing to disappear; 8, spermatozo5n just within the egg; v, germinal vesicle; vc, contents (extra chromosomal) of germinal vesicle. J, i/, first and second polar bodies; d*, sperm pronucleus; 9 , egg pronucleus.
chromatin, or the extra-chromosomal masses, which then disappear gradually into the cytoplasm while the small chromosomes pass into the division figure. Sometimes this loss of chromatin is effected by a shrinkage of the chromosomes themselves, as in some Elasmobranchs, where the chromosomes at this time shrink to about one-fortieth of their previous length and one-tenth their previous diameter (Ruckert, Fig. 34). Or the "nucleolus" of the oocyte may be a karyosome or chromatin nucleolus, and in such cases (Echinoderms, for example) during synizesis the chromatin may be nearly all contained within this body. Then the chromosomes are formed singly or in groups out of this "chromatin reservoir. After they have all been given off, much the greater part of the chromatin still remains in the karyosome, which then may fragment before dissolution, or it may be dissolved directly (Fig. 35). The subsequent behavior of the chromosomes is closely similar to that of' the spermatocyte chromosomes; tetrads may or may not be formed, according to the species, as the chromosomes pass into the division figure (Figs. 77, 78). The centrosome divides and the spindle and asters form typically in most respects save in size and position. The spindle is very, small and in most eggs is close to the surface of the cell at its animal pole (Fig. 76). In alecithal and isolecithal eggs the nucleus and spindle are at first located centrally and then later move to the periphery. At first the spindle lies parallel to a tangential plane, but during the mesophase it rotates through ninety degrees, putting its axis in a radial direction (Figs. 76, 77). In many cases the division of the oocyte is inhibited at this stage, until after the entrance of the spermatozoon, when it proceeds to completion; or this heterotype division may proceed without any interruption and the primary oocyte cut at once into two cells. The extremely eccentric position of the nucleus in this stage leads to one of the most characteristic features of oogenesis, namely, the very unequal division of the cell body. One of the products of division, the secondary oocyte, is of practically the same size as the primary oocyte; the other cell — the first polar body — is very much smaller, indeed usually minute (Figs. 76, 77, 78). In essentials these two daughters of the primary oocyte are equivalent ; their nuclei are alike in size and composition, each contains a daughter centrosome, but with the polar body th^re is only the smallest amount of cytoplasm and practically none of the deutoplasmic substance. The equal division of the nucleus is thus accomplished without appreciable loss from the oocyte of any of the cytoplasm and food reserve.
Fig. 77. — Maturation in the egg of Aicori* mtotUoeephaia bivaleiie. From Wilgon, "Cell," after BoverL A. Bgg with spepmato»o6n just entering at (?. The germinal vesicle contains two rod-shaped tetrads (only one clearly shown). B, C. Tetrads seen in profile and end views. D, First polar spindle forming (in this case within the genninBl vesicle). E. First polar spindle in definitive poeition. F. Tetrads dividing. O. First polar body formed, contatQing, like the egg, two dyads. H, I. Dyads rotating into portion for the aecond division. J. Dyads dividing. K. Each dyad has divided into two Bingie chromosomes, aa the second'polar division approaches. (For final stages, see Fig. 94.)
Fig. 78. — Diagram of reduction, with tetrad formation, in oogenesis^ From Wilson, *'Cell." The somatic number of chromosomes is supposed to be four. A, Initial phase; two tetrads have been formed in the germinal vesicle. B, The liwo tetrads have been drawn up about the spindle to form the equatorial plate of the first polar mitotic figure. C. The mitotic figure has rotated into position, leaving the remains of the germinal vesicle at gf.v. £>. Formation of the first polar body; each tetrad divides into two dyads. E. First polar body formed; two dyads in it and in the egg. F. Preparation for the second division. G. Second polar body forming and the first dividing; each dyad divides into two 49ingle chromosomes. H, Final result; three polar bodies and the egg-nucleus (9 ), each containing two single chromosomes (half the somatic number); c, the egg-centrofiome which now degenerates and is lost.
The second maturation or homotype division follows, either at once, or after a long pause in cases where the sperm normally enters at this time. The figure for the second maturation division is either a new figure or the reorganized remains of the preceding. In either case it appears in the region occupied by its predecessor, often in a radial position from its first appearance (Figs. 76, 77). Again the division is very unequal and the secondary oocyte gives rise to the large mature ovum and a small second polar body, again alike as regards nuclear composition. The first polar body may or may not divide into two at the same time; we may assume that such a division is normal, but on account of the degeneration of the polar bodies such a division tends to disappear; in different forms various stages of this division are reached. In a few rare instances, as in some Rotifers and Insects, the second polar body may also divide.
The chromosomes remaining in the ovum then re-form a reticular nucleus, smaller than the original oocyte nucleus, and with the haploid number of chromosomes; after forming a thin membrane the nucleus moves toward the cytoplasmic center of the ovum and there awaits union with the nucleus of the fertilizing spermatozoon (Figs. 76, 77). With few if any exceptions, the centrosome of the ovum is entirely lost as the nucleus is reconstructed; the absence of the centrosome is one of the peculiarities of the egg cell. It should be added that when the maturation is not completed until after the entrance of the sperm, the egg does not ordinarily re-form a typical nucleus but proceeds at once to unite with the sperm nucleus.
The final result of the two maturation divisions of the primary oocyte is the formation of four cells whose nuclei are similar, and which are morphologically exactly equivalent to one another (Figs. 74, 78). Physiologically, however, there is the greatest difference among them, since of the four only one, the ovum, is able to function, or indeed even to remain alive, and share in the development of a new organism. The other three (or two), the polar bodies, after a brief time degenerate and disappear.
The view that the ovum and the polar bodies are equivalent cells morphologically, and that the latter are in reality to be looked upon as degenerate egg cells (Mark) is now familiar. Their identity in nuclear structure and history i^ of course a decisive similarity.
Fig. 79. — ^Variations in the size of polar bodies, il, B, Sections through segmenting ovum of the Gasteropoda Limax maximufi^ showing polar bodies of very different sizes. After Meisenheimer. C-F. Ascaria megalocephala, C, D, E, after Sala, show influence of low temperature; F, after Boveri. C. Large first polar body which has divided. Z>. Very large first polar body. E. Equal division of egg during "first polar division." F, Equal division of egg during "second polar division." /, //• First and second polar bodies; 9, egg pronucleus; cf , sperm pronucleus.
The actual size of the polar bodies varies enormously. Those of the Echinoderms are among the smallest, some being only 5-8 micra (1/5000-1/3000 inch) in diameter; in Amphioxus they are about 7 micra, or about one-fourteenth the diameter of the egg, while in the mouse they are relatively much larger — 13 micray or one-fifth the diameter of the egg. An interesting series of forms can be arranged bridging over the si?e differences, and to some extent also the physiological differences between the ovum and the polar bodies. In a few Annelids, some Turbellaria, and most Molluscs (Fig. 79) the polar bodies are very large, sometimes even one-fourth the diameter of the egg itself. In occasional instances, abnormal "giant" polar bodies are formed, which really approach the ovum in size (e.gf., Amphioxus, and the Turbellarian, Prosthecercetts). Some of these large polar bodies form a definite membrane, like the vitelline membrane of the ovum; and in rare instances they are actually fertilizable, although their development never proceeds beyond an incomplete cleavage. The last step in the transition from polar body to egg cell is represented by an interesting condition occasionally found in Ascaris and some other forms, (e.g.f mouse) where an abnormally placed polar spindle may result in the division of the oocyte into two equal cells, one of which should be called a polar body (Fig. 79, E, F), The last step in the opposite direction — the dissimilarity between egg and polar body^ — ^reaches a climax in some of the Insects where polar bodies are not really formed as such; the o6c3i;e nucleus divides as in polar body formation and daughter nuclei are formed but these remain in the periphery of the egg cell, for no cytoplasmic division whatever is accomplished. The nuclear phase is the only part of the maturation division remaining. The "polar nuclei" formed in this way degenerate without sharing in development, just as if they had been cast out of the cell.
We have already suggested that this dissimilarity in size between the polar bodies and the ovum is in the nature of an adaptation such that maturation of the egg nucleus may take place without reducing the amount of cytoplasm and food materials which are to form the chief portion of the material basis of the new organism. In accomplishing this^ tliree of every four potential egg cells are totally deprived of these substances and lose all possibility of developing. In some few instances, the polar bodies may for a time remain alive and during the early cleavage show some signs of activity, such as the performance of amoeboid movement, "spinning activity," etc. (Andrews).
The location of the polar bodies within or without the vitelline membrane depends upon the time relation between membrane formation and maturation. The polar bodies may form before the membrane, in which case they usually are lost from the egg soon after their formation. More frequently they form after, and therefore within, the membrane and so can be seen for some time after development begins, when they form useful points for orientation, for in nearly all cases they mark the animal pole of the egg. The only exceptions to this location are among the Insects and Copepods, in which their position is variable.
Morphologically there is also complete correspondence between the ovum and the three polar bodies formed from the primary oocyte, and the four spermatids and spermatozoa formed from the primary spermatocyte (Platner, O.Hertwig). But again there is physiological divergence, in that all of the derivatives of the spermatocyte are capable of functioning as germ cells, while only one of the oocyte derivatives may do so. This physiological divergence is an expression, in another form, of the physiological division of labor between the egg and the sperm already referred to.
The chief points of similarity and difference between ovum and spermatozoon are summarized in the accompanying table.
Little is known regarding the nature of the stimuli which lead to the process of maturation, but it is clear that they are quite varied in different eggs. In some of those cases where the eggs are discharged freely into the water, contact with the water seems to initiate the process. 'But mati^ation may be begun previously to such a discharge. In some cases of this kind, as well as in others where the eggs are not thus freed, the rupture of the egg follicle seems to start the maturation process. In many cases the entrance of the sperm into the ovum is the effective stimulus to maturation, or to the completion of maturation in many of those instances where it has been begun previously and has been inhibited, either just before or just after the formation of the first polar body.
While we must postpone a part of our brief discussion of the theoretical significance of maturation, for ' reasons stated
Comparison op Typical Ovum and Spermatozoo'n
Similarities:
Nuclei contain the haploid number of chromosomes, the result of
two similar meiotic divisions. Chromosomes alike in form, size, and, with a few exceptions of
special significance, in number. Can function only after S3rngamy.
Differences:
Spermatozoon
Little cytoplasm. No deutoplasm.
Actively motile.
Centrosome present.
One of four similar products of the division of the spermatocyte, all of which are functional.
Usually completely formed and matured in the gonad.
Ovum
Much cytoplasm.
Nearly always contains deuto^ plasm, often very large amounts.
Non-motile.
Centrosome absent.
The functional one of four dissimilar products of the division of the o6c3rte, the other three of which are alike and not functional.
Usually formed but rarely completely matured in the gonad.
above, we should indicate at this time that the process has significance from at least two points of view. As a preliminary We should note that two different processes are involved in maturation; first, a reduction in the number of chromosomes, second, a reduction in the amount of chromatin. The earlier idea that maturation is merely a process by which the germ cells are rid of a part of their chromatin, and one-half of their chromosomes, as a preparation for the restoring union of chromatin and chromosomes during fertilization, is only one and probably the least important aspect. Many cells other than germ cells gain and lose large amounts of chromatin, and without going through any such complex process as that outlined above. Frequently much more than half, sometimes fully nine-tenths, of the chromatin is lost from the oocyte nucleus during maturation, while during spermatogenesis comparatively little may be lost. And the mere numerical reduction of chromosomes is fully accomplished in synapsis, before the actual maturation divisions occur. For these and many other reasons it seems that the chief importance of maturation is from the standpoint of inheritance. This is true particularly of most of the details regarding chromosome reduction, which become significant only when correlated with the facts, first, that the germ cells are the simplest phases in the life cycle of the organism, alternating with the mature phases, the complex characteristics of which are related to the simpler characters of the germ, and second, that in some way, as yet unknown, the structural and physiological characteristics of the new organism are, at least in part, primarily determined by the chromosomal structure of both of the germ nuclei, i.e., to the fact of biparental inheritance. From the standpoint of inheritance then the details of the behavior of the chromosomes during the maturation divisions take on the greatest importance. One of the more important matters is the precise plane of division of the chromosomes. It seems necessary to assume that each chromosome is not entirely homogeneous, but that its qualities differ in different parts. Consequently, in chromosomal composition the foiu* nuclei derived from each primary oocyte or spermatocyte nucleus may be all alike or may be of different kinds, according to whether the original chromosomes separated into similar or dissimilar parts in one or both of the* maturation divisions (Fig. 80) . In those cases where the chromosomes separate into qualitatively similar halves the division is said to be equationaly and when into qualitatively unlike halves the division is reducing. And it is commonly believed that one of the maturation divisions is equational and one reducing. When the equational division precedes, postreduction is said to occur; when the reducing division precedes it is described as prereduction (Korschelt and Heider). It is by no means a simple matter to determine whether a given chromosome division is equational or reducing, since there is externally visible no indication, in a chromosome itself, of its qualitative differentiation; and further because the processes of rearrangement and redistribution of the chromatin granules making up the chromosome axe usually very obscure, particularly when synizesis is pronounced.
This whole subject is in a rather more hypothetical state than one might wish, considering the importance of the con elusions to be drawn. Upon the assumption that the qualities of a chrompsome differ from end to end, a longitudinal fission of the chromosome would divide it into exactly similar halves, while a transverse fission would of course divide it dissimilarly. In many forms it is clear that the first or heterotype division is longitudinal and the second or homotype division is transverse so that the four resulting nuclei are of two categories. In other cases it appears superficially that both divisions are longitudinal, while in still others it is really impossible to say definitely whether a given division is longitudinal or transverse. A transverse division would be reducing, however, only upon the assumption of an end to end differentiation of the chromosome, and upon the finiiher assimiption, which should be clearly apprehended, that no rearrangement of the chromatin granules occurs during the maturation divisions. And the additional fact must be taken into consideration that the chromosomes of the primary spermatocyte or oocyte are bivalent, that they represent two chromosomes, which as wholes have fused in either parasynapsis or telosynapsis, and the actual chromatin granules composing them may have an arrangement in fusion which is not indicated by the behavior of the whole chromosome. The question whether a given longitudinal or transverse division of a chromosome is equational or reducing then can be determined only by taking all of these preliminary arrangements into account, and in most cases this is extremely difficult or even at present impossible. The small size of the chromosomes themselves and the minuteness, often invisibility, of the chromatin granules, often put the facts of their arrangement and behavior beyond the possibility of observation, and we can only infer their arrangement and history from subsequent events. In most cases we know only that reduction occurs. And from the few cases in which the course of events seems clear, we infer that in all maturation divisions, one is equational, one reducing, resulting in the fonnation of germ cells of two more or less unlike kinds, in equal numbers (Fig. 80).
Fig, 80. — Diagrams representing the behavior of the chromosomes during fertilization and maturation. The differentiation of the three kinds of chromosomes is indicated by the number of small circles in each, c^, chromosomes derived from the spermatozoon (sperm pronucleus) (black circles) ; 9 * those from the egg (egg pronucleus) (white circles). The somatic number of chromosomes is six. A. Entrance of spermatozodn. B, Fusion of egg and sperm pronuclei, forming the first cleavage nucleus. C. Splitting of chromosomes in equatorial plate, during the division of any somatic, odgonial, or spermatogonial cell. D. Primary odcyte or spermatocyte in synapsis (telosynapsis). Fusion of similar chromosomes of maternal and paternal origin. E. Longitudinal splitting of bivalent chromosomes during first maturation division. F. First division completed forming the two secondary o5cytes or spermatocytes. The nuclei are alike in composition. O, Transverse division of chromosomes during second maturation division (reducing division — postreduction). H. The resulting four cells. With respect to each chromosome the cells are of two kinds, numerically equal.
Aside from its relation to the phenomena of heredity, the meaning of the maturation process is very problematic. In the Protozoa where definite chromosomes are formed only infrequently, maturation frequently involves a separation between reproductive and vegetative chromatin, as already suggested. Among the Metazoa there is usually a loss of chromatin from the nucleus, but it is very doubtful whether it has a similar meaning. In a great many cells, particularly those which are very active, e.g., gland cells, oocytes, etc.y the cytoplasm is constantly receiving substance from the nucleus. This material is frequently chromatic, and the granules of this kind have received a variety of special names, but collectively may be included under the term chromidia. (See Chapter II.) It may be that through some such process as this the nucleus exercises those forms of control and regulation of cell life that are its chief function. The loss and degeneration of the chromatin distributed to the polar bodies can have no significance here, for that process is involved in the degeneration of the entire polar bodies, which has an entirely dilerent meaning. But dx^ng the groUh period of most ova, just after synizesis, a relatively large amount of the chromatin is thrown out into the cytoplasm, and during the later stages of spermatogenesis a somewhat similar loss may be observed. And in the very early history of the germ cells of the organism, when this may consist of only a few cells, the primordial germ cells may often be distinguished by just this process of chromatin discharge from the nucleus. Such cells are often characterized by unusually large nuclei, and a large fraction of their chromatin content may be liberated into the cytoplasm at each mitosis. It may very well be, therefore, that this is a regular and highly significant process in the formation and maturation of the germ cells, having to do with the unusual activity of the sperm or with the development of various formed substances, both protoplasmic and deutoplasmic, present in the cytoplasm of the ovum. Indeed it may not be too much to suppose that the all-importaDt "organization" of the ovum may in some way be related to this process of chromatin distribution.
The fact of tnaturstioQ has been determined for all groups of manycelled aoimalB and plants, and among the unicellular forms it is by no means uncommon. Among the Protozoa the phenomena of maturation are of considerable theoretical interest. In those forms in which the chromatin is not formed into definite chromosomes, but remains unorganized, grossly, there seems to be a kind of division of labor between vegetative and kinetic (reproductive) forms of chromatin. The reproductive nuclei (idiochromidia) are frequently distinctly separate from the somatic nuclei (chromidia), and just before fertilization the former may divide twice in rapid succession. This process bears the greater resemblance to the maturation of the ovum since after each division one of the two products degenerates, often without actually being thrown out of the cell, leaving functional only one of the four products of the original idiochromidium. Actinoaphwrium is a tjrpical example (R. Hertwig), and there are several other forms where much, the same thing occurs, «.?., Actinophrys (Fig. 81), Entanmba. In all caaea such as these, it is impossible to say whether reduction, in a strict sense, is accomplished, or whether thia is merely an elimination of chromatin, for the chromatin is not organiaed into chromosomes whose precise behavior may be traced; it is quite likely that there is here no true reduction in the MetaEoan sense. In some of the Infusoria, however, definite chromosomes are formed in the nucleus during these divisions and a definite chromosomal history may be made out. In Parammcium, for instance, as described by Calkins and Cull, where the idiochromidia are known aa the mtcronwciei, these alone are concerned in the " maturation " divisions. The mieronucleua forms a fairly typical division figure consiating of a spindle and more than 200 separate chromosomes. During the first maturation division each of these divides longitudinally, the resultants passing in each case to the separate daughter nuclei, without any corresponding division of the cell body (Fig, 82). A second maturation division foEows immediately and is precisely like the first giving four daughter nuclei (micronuclei, idiochromidia), three of which then degenerate as in polar body formation. The one remaining nucleus divides agtun, this time the chromosomes dividing transversely (reducing division?). This third division is not strictly comparable with anything to be found in the Metazoa and is apparently correlated with the character of the fertilization process in this form, for both parts share in reproduction. One-half remains in situ as the equivalent (analog) of the egg nucleus, and the other half migrates, as the equivalent (analog) of the^ aperm nucleus, to the body of another organism, fusing with (fertilizing) the stationary nucleus of that individual. In the majority of theProtozoa the so-called "maturation" or "reduction" divisions are not equivalent to these processes in the Metaioa, but are merely dimions by which a separation is effected between the reproductive and nutritive chromatin, i.e., idiochromatin and trophochromalin; in nearly all known forms only the former takes any active part in the subsequent reproductive processes, while the trophochromatin usually dissolves and disappears.
Fig. 81. — Maturation phenomena accompanying conjugation in the Rlii«opod, Actinopkrye tot. From Calkioa, "Protniua," after Schaudinn. A. Farts of two individuals, fused; the axial GlameDts terminate in granules on the surface of the nucleus. B. Nuclei in prophase. C Formation of first polar spindle. Z>. Reconstruction of nuclei. E. Fusion of nuclei. F. First division spindle. p, polar body,
Fig. 82. — Maturation divisiooa in Paramacium aureltn (eawfalum). Ftom Calkina and CuU. Only a few of the chromosomes are represented in each case. A. Late anaphase of first maturation diviaion of micronucleus; some chtomoBomea incompletely divided. X 1000. B. Early auaphaae of second maturation division, x 633. C. Telophase of second maturation division. X 900.
Two very special modifications of the maturation process deserve just a word. The first is in connection with those few eggs which normally develop without fertilization (parthenogenesis), i.e., without the union of equivalent egg and sperm nuclei. In such cases, which are known in the Aphids, many Crustacea, and Rotifers, for example, the normal course of maturation would lead to the formation of an organism with the haploid number of chromosomea (^\ in all of its cells. In most, if not in all, such cases which have been studied, it Is now known that as a matter of fact the egg is not left with the reduced number of chromosomes. Thus in. the brine-shrimp, Artemia (Brauer), which illustrates the usual course of events in parthenogenesis, the first maturatJon division proceeds as usual and is equational (reducing), leaving ^ bivalent chromosomes in the secondary o6cyte nucleus. Then one of two courses may be followed (Fig. 83). In most normally partheno genetic eggs a. second polar body is foimed typically, leaving the reduced number of univalent chromosomes in the egg nucleus, but then the second polar body immediately reenters the egg, apparently taking the place of an equivalent sperm nucleus and restoring the chromosomal characters to the normal somatic condition, after which development proceeds. The polar body need not be actually extruded from the egg cell in order to give the same history, as long as the nuclear events are equivalent (Fig. 84) . In some eggs, even of species in which the history is at times similaj to that just described, a different method gives the same result. Thus,, while the second polar spindle may form typically, the chromosomes upon it do not divide, and the equivalent of the second polar nucleus is never formed. The egg nucleus then re-forms with its = chromosomes, but these are bivalent as shown by the character of the first maturation division, so that in effect the e^ nucleus contains the somatic number of chromosomes, which actually appears in subsequent divisions. It is therefore clear that while such parthenogenetic ^gs fail to receive a sperm nucleus they retain or receive back the equivalent of such a nucleus in the form of the second polar body nucleus, which ia not lost as it is in eggs requiring to be fertilized.
Fig. 83. — MBturatioQ ia the partheDogenetio ege oi the brine-Bbrinip, ATtemia. After Brauer. A, X 796^ others. X 368. A. Second polar body incompletely cut off. B. Second polar nucleus refintericg the egg and approaching the egg pronucleuB. C. D. Fusion of second polar body nucleus with egg pronucleus. E, Firat cleavage spindle with two groupe of chromoaomeB derived from the two nuclei. II, Second polar body oi nucleus; 9, egg pronucleus.
Fig. 84. — Maturation in the parthenoseneUc egg of the Echiiiodenii, Atlro' pecten. After O. Hertwig. A. First polar body formed but not extruded; iecond polar division in early anaphSBe. B, First polar body extruded; second polar division completed, the polar nucleus near the periphery. C, D, B. Stages In tbe gradual approach and fusion of the second polar nucleus and egg pronucleus, to Form the cleavage nucleus. I. First polar body; II, second polar nucleus; 9 , egg pronucleus.
The second unusual modification of maturation is to be seen in the spermatogenesis of many Arthropods, chiefly Insects. These species have abeady been mentioned as showing a numerical difference between the chromosome groups of the male and female individuals, the female having, in different species, one or several chromosomes more than the male. In these forms the first maturation division is typical and the two secondary spermatocytes are similar. But the second maturation division is asymmetrical in that one or more chromosomes known as the accessory or idiochromosomes fail to divide and are therefore distributed to only one-half of the spermatids and spermatozoa. Half of the sperm cells then have ^ chromosomes, the other half ^ plus one, or more aa the case may be in different species. These striking phenomena and their relation to the question of sex determination are described more fully in Chapter VII.
In conclusion we should mention briefly the place of the maturation divisions in the life histories of different organisms. In any many-celled organism the life cycle as a whole may be said to consist of two phases, one characterized by the possession of the diploid chromosome group, the other by the haploid group. Among all of the Metazoa, and many of the Protozoa, there are invariably only two cell generations with the haploid number, and further, these always are the two final generations in the process of gametogenesis. Here they seem bound up with the process of fertilization and are to be understood only from the point of view of what is involved in this process. Considering these forms alone it is difficult to understand how it should have come about that numerical reduction of the chromosomes should occur in advance of the condition out of which arose the necessity for reduction,'namely, the fusion of the germ nuclei. But this arrangement is by no means invariable. In Amceha diploidea (Hartmann and Nagler) reduction does actually occur after conjugation. And in some of the lower plants, such as many of the green AlgsB (Chlorophycese), the relation between fertilization and numerical reduction is that which apparently must have been the more primitive. In these forms the gametic nuclei contain the same number of chromosomes (s) as do the somatic or vegetative cells; these fuse forming a zygote with double this number (2s). This fusion is then followed immediately by two maturation divisions, the first of which is usually heterotypic, which result in the formation of four cells, each again with the original vegetative number (s). Certain or all of these four cells then produce the body of the new organism, all the cells of which, including the germ cells when these form, have this same chromosome number (s). That is, numerical reduction of the chromosomes follows syngamy, a relation which seems more understandable than the more* common precedence of reduction. In describing cases like these we might say that the somatic or vegetative cells and the germ cells all have the haploid chromosome group. In fertilization the diploid group is formed, but is then retained through only two generations, after which the haploid condition is restored. In other words the predominating stage in the Ufe cycle is that with the haploid chromosome group, the diploid group occurring only in the divisions following fertilization; "haploid" is here sjmonymous with "somatic."
In many other plants, such as the ferns and mosses among others, the life cycle is more equally divided into two distinct periods, one carried on with the haploid (in the usual sense of the word), one with the diploid chromosome group. The cells of the fern while it is in the typical "fern-plant" stage. have the diploid group, but during the formation of spores by this plant, reduction occurs, the reduced number appearing in the spore mother cell. And in all of the cells of the prothallus, derived from the spore, the haploid number remains; no further reduction occurs when the prothallus forms gametes. The diploid number is only restored by the union of two gametes in the formation of the new fern plant, throughout the exiistence of which it is retained. It is a matter of considerable theoretical interest that the familiar alternation between the sporophyte and gametophyte generations, between fern plant and prothallus, for example, should be accompanied by a corresponding alternation between the diploid and haploid chromosome groups. We may relate this to the condition in the green Algse by saying that the number of cell generations following fertilization, in which the diploid chromosomes are retained, is greatly increased and the number with the haploid group correspondingly diminished, indeed in most cases here, the diploid stage is of greater duration than the haploid. In the higher plants (Gymnosperms and Angiosperms) it is agreed that the prothallus, i.e., the stage with the haploid chromosome group, is represented only by certain vestiges — the pollen tube and embryo sac, and it is significant that here, after the two maturation divisions leading to the lormation of the germ cells, two or more (but never more than a few) additional divisions occur giving rise to these vestiges; the haploid chromosome number is found in all of these divisions. Here then the phase with the reduced number of chromosomes is still more limited — practically to the extent found in animals. And whereas in the lower plants the diploid stage is restricted to two cell generations, in the higher plants it is the haploid stage which comes to be so limited.
Many consider the gametophyte generation, t.e., the prothallus, or its equivalent in other forms, as the primary form or phase; consequently they regard the number of chromosomes in the cells of this phase, the haploid number, as primitive or normal, and not as a reduced number. Correspondingly the diploid number would result from a douhlingy not from a restoring of the normal. The development of this point of view in connection with the conditions in the higher plants (Strasburger) has led to the suggestion (Whitman) that even in animals the number of chromosomes in the secondary oo- and spermatocytes and mature germ cells, i.e,, the haploid number, is again in reality the normal, that this is doubled in fertilization, and remains doubled throughout the somatic divisions, only to be again reduced to normal by the subsequent maturation divisions. Upon this hypothesis, which also explains the present precedent relation of maturation to fertilization, the two cell generations immediately preceding fertilization are all that remain of the primary phase of the animal life cycle.
The alternation between the sporophyte and gametophyte in ferns and mosses is truly an alternation of generations and we may thus see an alternation of generations even in the higher plants where there may be a total of only four divisions with the haploid number — the normal according to some. If this is allowed, it is possible that in animals where there are but two of these corresponding cell divisions, we might still speak of an alternation of generations as well; the equivalent of the gametophyte would then be represented, vestigially, only by the cells with the haploid chromosome group, i.e., primary and secondary ooahd spermatocytes which form the gametes proper — and the equivalent of the sporophyte generation would be represented by all the remaining generations of cells which we commonly think of as the true organism, and which forms " asexually " the 06- and spermatogonia — the equivalents then of the spore mother cells. Of course in animals the matter is complicated greatly by the separation of the two sexes as two separate individuals. Such a comparison as this must remain, at least for the present, as an interesting speculation merely, for none of the Metazoa offers any variations in the maturation process which shed any light upon the comparison.
References to Literature
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cephala. Arch. mikr. Anat. 42. 1893. Zur Kenntniss der Rei fung des parthenogenetisch sich entwickelnden Eies von Artemia
scUina, Arch. mikr. Anat. 43. 1894. Calkins, G. N., and Cull, S. W. (See ref. Ch. II.) Cardiff, I. D., A Study of Sjmapsis and Reduction. Bull. Torrey
Botan. Club. 33. 1906. CoE, W. R., The Maturation and Fertilization of the Egg of Cerebraiultis.
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Davis, B. M., Nuclear Phenomena of Sexual Reproduction in Algse.
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(Anat. Abth.). 1907. Gates, R. R., The Mode of Chromosome Reduction. Botan. Gaz. 51.
1911. GrjIooire, v., Les Cin^ses de maturation dans les deux r^gnes. L'unit4
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n. sp., etc. Sitz.-Ber. Ges. Nat. Freunde. Berlin. 4. 1908. Hertwio, O., Beitrage zur Kenntniss der Bildimg, Befruchtung und
Teilimg des Tierischen Eies. I. Morph. Jahrb. 1. 1875. Jordan, H. E., The Spermatogenesis of the Opossum (Didelphys vir^
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the Chondriosomes. Arch. Zellf. 7. 1911. KoRSCHBLT UND Heider, Lchrbuch, etc. (See ref. Ch. III.) McClung, C. E., The Chromosome Complex of Orthopteran Spermatocytes. Biol. Bull. 9. 1905. Montgomery, T. H.^ Jr., The Heterotypic Maturation Mitosis in
Amphibia and its General Significance. Biol. Bull. 4. 1903.
(See also ref. Ch. II, III.) Morse, M. W., The Nuclear Components of the Sex Cells of four Species
of Cockroaches. Arch. Zellf. 3, 1909. Platnbr, G., (See ref. Ch. III.)
ScHAFFNER, J. H., S3aiapsis and Synizesis. Ohio Naturalist. 7. 1907. Sch5nfeld, H., La Spermatog^n^e chez le taureau et chez le mam mif^res en g^n^ral. Arch. Biol. 18. 1901. de Sin£ty, R., Recherches sur la Biologie et Tanatomie des Phasmes.
CeUule. 19. 1901. Strasburger, E., Ueber periodische Reduktion der Chromosomenzahle
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English Translation in Annals Botany. 8. 1895. Ueber Reduk tionsteilung. Sitz.-Ber. Akad. Wiss. Berlin. 1904. Wilson, E. B., (See ref. Ch. II.) Winiwarter, H. v., Recherches sur Fovogen^se et organogen^se de
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1900. (See also Anat. Anz. 21. 1902.) Winiwarter, H. v., and Sainmont, G., Nouvelles recherches sur
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Kellicott WE. A Textbook of General Embryology (1913) Henry Holt and Co., New York.
Kellicott (1913): 1 Ontogeny | 2 The cell and cell division | 3 The germ cells and their formation | 4 Maturation | 5 Fertilization | 6 Cleavage | 7 The germ cells and the processes of differentiation, heredity, and sex determination | 8 The blastxtla, gastrula, and germ layers. Morphogenetic processes
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