Opening
THE WORKS
OF
FRANCIS MAITLAND BALFOUR.
VOL. II.
Memorial Edition.
Cambridge:
PRINTED BY C. J. CLAY, M.A. AND SON, AT THE UNIVERSITY PRESS.
Memorial Edition.
THE WORKS
OF
FRANCIS MAITLAND BALFOUR,
M.A., LL.D., F.R.S., FELLOW OF TRINITY COLLEGE, AND PROFESSOR OF ANIMAL MORPHOLOGY IN THE UNIVERSITY OF CAMBRIDGE.
EDITED BY
M. FOSTER, F.R.S., PROFESSOR OF PHYSIOLOGY IN THE UNIVERSITY OF CAMBRIDGE;
AND
ADAM SEDGWICK, M.A., FELLOW AND LECTURER OF TRINITY COLLEGE, CAMBRIDGE.
VOL. II.
A TREATISE ON COMPARATIVE EMBRYOLOGY.
Vol. I. Invertebrata.
London: MACMILLAN AND CO. 1885
[The Right of Translation is reserved.]
Preface
My aim in writing this work has been to give such an account of the development of animal forms as may prove useful both to students and to those engaged in embryological research. The present volume, save in the introductory chapters, is limited to a description of the development of the Invertebrata: the second and concluding volume will deal with the Vertebrata, and with the special histories of the several organs.
Since the work is, I believe, with the exception of a small but useful volume by Packard, the first attempt to deal in a complete manner with the whole science of Embryology in its recent aspects, and since a large portion of the matter contained in it is not to be found in the ordinary text books, it appeared desirable to give unusually ample references to original sources. I have accordingly placed at the end of each chapter, or in some cases of each section of a chapter, a list of the more important papers referring to the subject dealt with. The papers in each list are numbered continuously, and are referred to in the text by their numbers. These lists are reprinted as an appendix at the end of each volume. It will of course be understood that they do not profess to form a complete bibliography of the subject.
In order to facilitate the use of the work by students I have employed two types. The more general parts of the work are printed in large type; while a smaller type is used for much of the theoretical matter, for the details of various special modes of development, for the histories of the less important forms, and for controversial matter generally. The student, especially when commencing his studies in Embryology, may advantageously confine his attention to the matter in the larger type; it is of course assumed that he already possesses a competent knowledge of Comparative Anatomy.
Since the theory of evolution became accepted as an established doctrine, the important bearings of Embryology on all morphological views have been universally recognised: but the very vigour with which this department of science has been pursued during the last few years has led to the appearance of a large number of incomplete and contradictory observations and theories; and to arrange these into anything like an orderly and systematic exposition has been no easy task. Many Embryologists will indeed probably hold that any attempt to do so at the present time is premature, and therefore doomed to failure. I must leave it to others to decide how far my effort has been justified. That what I have written contains errors and shortcomings is I fear only too certain, but I trust that those who are most capable of detecting them will also be most charitable in excusing them.
The work is fully illustrated, and most of the figures have been especially engraved from original memoirs or from my own papers or drawings by Mr Collings, who has spared no pains to render the woodcuts as clear and intelligible as possible. I trust my readers will not be disappointed with the results. The sources from which the woodcuts are taken have been in all cases acknowledged, and in the cases where no source is given the illustrations are my own.
I take this opportunity of acknowledging my great obligations to Professors Agassiz, Huxley, Gegenbaur, Lankester, Turner, Kölliker, and Claus, to Sir John Lubbock, Mr Moseley, and Mr P. H. Carpenter, for the use of electrotypes of woodcuts from their works.
I am also under great obligations to numerous friends who have helped me in various ways in the course of my labour. Professor Kleinenberg, of Messina, has read through the whole of the proofs, and has made numerous valuable criticisms. My friend and former pupil, Mr Adam Sedgwick, has been of the greatest assistance to me in correcting the proofs. I have had the benefit of many useful suggestions by Professor Lankester especially in the chapter on the Mollusca, and Mr P. H. Carpenter has kindly revised the chapter on the Echinodermata.
I am also much indebted to Dr Michael Foster, Mr Moseley, and Mr Dew-Smith for aid and advice.
CONTENTS OF VOLUME I.
INTRODUCTION. Pp. 1-16.
I. THE OVUM AND SPERMATOZOON
General history of the Ovum, pp. 17-25. Special history of the Ovum in different types, pp. 26-65. The Spermatozoon, pp. 65-67.
II. THE MATURATION AND IMPREGNATION OF THE OVUM
Maturation of the Ovum, and formation of the polar bodies, pp. 68-79. Impregnation of the Ovum, pp. 79-86. Summary, p. 86.
III. THE SEGMENTATION OF THE OVUM
Internal phenomena of Segmentation, pp. 88-92. External features of Segmentation, pp. 92-122.
INTRODUCTION TO SYSTEMATIC EMBRYOLOGY. Pp. 125-130.
VI. COELENTERATA
Hydrozoa, pp. 152-167. Actinozoa, pp. 167-173. Ctenophora, pp. 173-178. Summary, etc., pp. 178-182. Alternations of generations, pp. 182-187.
VII. PLATYELMINTHES
Turbellaria, pp. 189-196. Nemertea, pp. 196-204. Trematoda, pp. 205-210. Cestoda, pp. 210-218.
IX. MOLLUSCA
Formation of the layers and larval characters, pp. 225-273. Gasteropoda and Pteropoda, pp. 225-242. Cephalopoda, pp. 242-254. Polyplacophora, pp. 254-257. Scaphopoda, pp. 257, 258. Lamellibranchiata, pp. 258-269. _General review of Molluscan Larvæ_, pp. 270-273. Development of organs, pp. 273-288.
X. POLYZOA
Entoprocta, pp. 292-297. Ectoprocta, pp. 297-305. Summary and general considerations, pp. 305-308.
XI. BRACHIOPODA
Development of the layers, pp. 311-313. The history of the larva, pp. 313-317. Development of organs, p. 317. General observations on the affinities of the Brachiopoda, pp. 317, 318.
XII. CHÆTOPODA
Formation of the germinal layers, pp. 319-325. The larval form, pp. 325-338. Formation of organs, pp. 338-342. Alternations of generations, pp. 342, 343.
XIII. DISCOPHORA
Formation of layers, pp. 347-350. History of larva, pp. 351-354.
XIV. GEPHYREA
Gephyrea nuda, pp. 355-361. Gephyrea tubicola, pp. 361-364. General considerations, p. 364.
Chapter XV
Chætognatha, pp. 366-369. Myzostomea, pp. 369, 370. Gastrotricha, p. 370.
Chapter XVI
Nematelminthes, pp. 370-379. Acanthocephala, pp. 379-381.
XVII. TRACHEATA
Prototracheata, pp. 382-387. Myriapoda, pp. 387-395. Insecta, pp. 395-429. Embryonic membranes and the formation of the layers, pp. 400-406. Formation of the organs, pp. 406-417. Special types of larvæ, pp. 417-419. Metamorphosis and heterogamy, pp. 420-429. Arachnida, pp. 431-455. Formation of the layers and general development, pp. 431-446. Formation of the organs, pp. 446-455. Formation of the layers and embryonic envelopes in the Tracheata, pp. 456-458.
XVIII. CRUSTACEA
History of larval forms, pp. 459-511. Branchiopoda, pp. 459-465. Malacostraca, pp. 465-487. Copepoda, pp. 487-492. Cirripedia, pp. 492-500. Ostracoda, pp. 500-502. Phylogeny of the Crustacea, pp. 502-511. The formation of the germinal layers, pp. 511-521. Comparative development of organs, pp. 521-529.
Chapter XIX
Poecilopoda, pp. 534-538. Pycnogonida, pp. 538, 539. Pentastomida, pp. 539-541. Tardigrada, p. 541. Summary of Arthropodan Development, pp. 541-543.
XX. ECHINODERMATA
Development of the germinal layers, pp. 544-553. Development of the larval appendages and metamorphosis, pp. 553-573. Summary and general considerations, pp. 573-576.
XXI. ENTEROPNEUSTA. Pp. 579-583
INDEX. Pp. 584-590.
Appendix
EMBRYOLOGY.
Introduction
Embryology forms a large and important department of Biology. Strictly interpreted according to the meaning of the word, it ought to deal with the growth and structure of organisms during their development within the egg membranes, before they are capable of leading an independent existence. Modern investigations have however shewn that such a limitation of the science would have a purely artificial character, and the term Embryology is now employed to cover the anatomy and physiology of the organism during the whole period included between its first coming into being and its attainment of the adult state.
The subject-matter of the science of Embryology admits of a twofold classification. It may be placed under a series of heads, each dealing either with a special group of organisms, or with a special department of the whole science. If classified in the first of these ways the science will naturally be divided into an Embryology of Plants, and an Embryology of Animals; each of which admits of further subdivision. In the second way the subject falls under two primary heads; viz. Physiological Embryology and Anatomical Embryology.
The present treatise deals only with the Embryology of Animals, and is further confined to those animals known as Metazoa. The science is moreover treated from the morphological or anatomical, rather than from the physiological side.
The marvellous phenomenon of the evolution of a highly complicated living being from a simple undifferentiated germ in which it needs the aid of the most modern microscopical appliances to detect any visible signs of life, has not unnaturally attracted the attention of biologists from the very earliest periods. Before the establishment of the cell theory the origin of the organism from the germ was not known to be an occurrence of the same nature as the growth of the fully formed individual, and Embryological investigations were mixed up with irrelevant speculations on the origin of life[1].
[1] To this general statement Wolff forms a remarkable exception, for though without any clear knowledge of what we call cells he had very distinct notions on the relations of growth and development.
The difficulties of understanding the formation of the individual from the structureless germ led anatomists at one time to accept the view "according to which the embryo preexisted, even though invisible, in the ovum, and the changes which took place during incubation consisted not in a formation of parts, but in a growth, i.e. in an expansion with concomitant changes of the already existing germ."
Great as is the interest attaching to the simple and isolated life histories of individual organisms, this interest has been increased tenfold by the generalizations of Mr Charles Darwin.
It has long been recognized that the embryos and larvæ of the higher forms of each group pass, in the course of their development, through a series of stages in which they more or less completely resemble the lower forms of the group[2]. This remarkable phenomenon receives its explanation on Mr Darwin's theory of descent. There are, according to this theory, two guiding, and in a certain sense antagonistic principles which have rendered possible the present order of the organic world. These are known as the laws of heredity and variation. The first of these laws asserts that the characters of an organism at all stages of its existence are reproduced in its descendants at corresponding stages. The second of these laws asserts that offspring never exactly resemble their parents. By the common action of these two principles continuous variation from a parent type becomes a possibility, since every acquired variation has a tendency to be inherited.
[2] Von Baer who is often stated to have established the above generalization really maintained a somewhat different view. He held (Ueber Entwickelungsgeschichte d. Thiere, p. 224) that the embryos of higher forms never resembled the adult stages of lower forms but merely the embryos of such forms. Von Baer was mistaken in thus absolutely limiting the generalization, but his statement is much more nearly true than a definite statement of the exact similarity of the embryos of higher forms to the adults of lower ones.
The remarkable law of development enunciated above, which has been extended, especially by the researches of Huxley[3] and Kowalevsky, beyond the limits of the more or less artificial groups created by naturalists, to the whole animal kingdom, is a special case of the law of heredity. This law, interpreted in accordance with the theory of descent, asserts that each organism in the course of its individual ontogeny repeats the history of its ancestral development. It may be stated in another way so as to bring out its intimate connection with the laws of inheritance and variation. Each organism reproduces the variations inherited from all its ancestors at successive stages in its individual ontogeny which correspond with those at which the variations appeared in its ancestors. This mode of stating the law shews that it is a necessary consequence of the law of inheritance. The above considerations clearly bring out the fact that Comparative Embryology has important bearings on Phylogeny, or the history of the race or group, which constitutes one of the most important branches of Zoology.
[3] Huxley was the first to shew that the body of the Coelenterata was formed of two layers, and to identify these with the two primary germinal layers of the Vertebrata.
Were it indeed the case that each organism contained in its development a full record of its origin, the problems of Phylogeny would be in a fair way towards solution. As it is, however, the law above enunciated is, like all physical laws, the statement of what would occur without interfering conditions. Such a state of things is not found in nature, but development as it actually occurs is the resultant of a series of influences of which that of heredity is only one. As a consequence of this, the embryological record, as it is usually presented to us, is both imperfect and misleading. It may be compared to an ancient manuscript with many of the sheets lost, others displaced, and with spurious passages interpolated by a later hand. The embryological record is almost always abbreviated in accordance with the tendency of nature (to be explained on the principle of survival of the fittest) to attain her ends by the easiest means. The time and sequence of the development of parts is often modified, and finally, secondary structural features make their appearance to fit the embryo or larva for special conditions of existence. When the life history of a form is fully known, the most difficult part of his task is still before the scientific embryologist. Like the scholar with his manuscript, the embryologist has by a process of careful and critical examination to determine where the gaps are present, to detect the later insertions, and to place in order what has been misplaced.
The aims of Comparative Embryology as restricted in the present work are two-fold: (1) to form a basis for Phylogeny, and (2) to form a basis for Organogeny or the origin and evolution of organs. The justification for employing the results of Comparative Embryology in the solution of the problems in these two departments of science is to be found in the law above enunciated, but the results have to be employed with the qualifications already hinted at; and in both cases a knowledge of Comparative Anatomy is a necessary prelude to their application.
In accordance with the above objects Comparative Embryology may be divided into two departments.
The scientific method employed in both of these departments is that of comparison, and is in fact fundamentally the same as the method of Comparative Anatomy. By this method it becomes possible with greater or less certainty to distinguish the secondary from the primary or ancestral embryonic characters, to determine the relative value to be attached to the results of isolated observations, and generally to construct a science out of the rough mass of collected facts. It moreover enables each observer to know to what points it is important to direct his attention, and so prevents that simple accumulation of disconnected facts which is too apt to clog and hinder the advance of the science it is intended to promote.
In the department of Phylogeny the following are the more important points aimed at.
(1) To test how far Comparative Embryology brings to light ancestral forms common to the whole of the Metazoa. Examples of such forms have been identified by various embryologists in the ovum itself, supposed to represent the unicellular ancestral form of the Metazoa: in the ovum at the close of segmentation regarded as the polycellular Protozoon parent form: in the two-layered gastrula, etc., regarded by Haeckel as the ancestral form of all the Metazoa[4].
[4] The value of these identifications as well as of those below is discussed in its appropriate place in the body of the work. Their citation here is not to be regarded as necessarily implying my acceptance of them.
(2) How far some special embryonic larval form is constantly reproduced in the ontogeny of the members of one or more groups of the animal kingdom; and how far such larval forms may be interpreted as the ancestral type for those groups.
As examples of such forms may be cited the six-limbed Nauplius supposed by Fritz Müller to be the ancestral form of the Crustacea; the trochosphere larva of Lankester, which he considers to be common to the Mollusca, Vermes, and Echinodermata; the planula of the Coelenterata, etc.
(3) How far such forms agree with living or fossil forms in the adult state; such an agreement being held to imply that the living or fossil form in question is closely related to the parent stock of the group in which the larval form occurs. It is not easy to cite examples of a very close agreement of this kind between the larval forms of one group and the existing or fossil forms of another. The larvæ of some of the Chætopoda with long provisional setæ resemble fossil Chætopods. The Rotifers have many points of resemblance to the trochosphere, especially to that form of trochosphere characteristic of the Mollusca. The Turbellarians have some features in common with the Coelenterate planula. Some of the Gephyrea in the presence of a præoral lobe resemble certain trochosphere types. The larva of the Tunicata has the characters of a simple type of the Chordata.
Within the limits of a single group agreements of this kind are fairly numerous. In the Craniata the tadpole of the Anura has its living representative in the Pisces and perhaps especially in the Myxinoids. The larval forms of the Insecta approach Peripatus. The stalked larva of Comatula is reproduced by the living Pentacrinus and Rhizocrinus etc. Numerous examples of the same phenomenon are found amongst the Crustacea.
(4) How far organs appear in the embryo or larva which either atrophy or become functionless in the adult state, and which persist permanently in members of some other group or in lower members of the same group. Cases of this kind are of the most constant occurrence, and it is only necessary to cite such examples as the gill slits and Wolffian body in the embryos of higher Craniata to illustrate the kind of instance alluded to. The same conclusions may be drawn from them as from the cases under the previous heading.
(5) How far organs pass in the course of their development through a condition permanent in some lower form. Phylogenetic conclusions may be drawn from instances of this character, though they have a more important bearing on Organology than on Phylogeny.
The considerations which were used to shew that the ancestral history is reproduced in the ontogeny of the individual apply with equal force to the evolution of organs. The special questions in Organology, on which Comparative Embryology throws light, may be classified under the following heads.
(1) The origin and homologies of what are known as the germinal layers; or the layers into which the embryo becomes divided immediately after the segmentation.
(2) The origin of primary tissues, epithelial, nervous, muscular, connective, etc., and their relation to the germinal layers.
(3) The origin of organs. The origin of the primitive organs is intimately connected with that of the germinal layers. The first differentiation of the segmented ovum results in the cells of the embryo becoming arranged as two layers, an outer one known as the epiblast and an inner one as the hypoblast. The outer of these forms a primitive sensory organ, and the inner a primitive digestive organ.
(4) The gradual evolution of the more complicated organs and systems of organs.
This part of the subject, even more than that dealing with questions of Phylogeny, is intimately bound up with Comparative Anatomy; without which indeed it becomes quite meaningless.
REPRODUCTION.
A study of reproduction logically precedes that of Embryology. Reproduction essentially consists in the separation of a portion of an organism which has the capacity of developing into a form similar to that which gave it origin. The simplest modes of reproduction are those which occur amongst the Protozoa.
In this group, reproduction may take place in a great variety of ways. These may be classified in three groups: (1) fission, (2) budding or gemmation, (3) spore formation.
Reproduction in all these ways may take place either subsequently to and apparently in consequence of a very important process known as conjugation, which consists in the temporary or permanent fusion of two or more individuals, or spontaneously, i.e. independently of any such previous conjugation.
Reproduction by fission consists simply in the division of the organism into two similar parts, the nucleus when present becoming divided simultaneously with the cell body. This mode of reproduction is the simplest conceivable, and is not followed by a development, since the two organisms produced are exactly similar, except in size, to the parent form. Besides single fission, a process of multiple fission may take place, as amongst the Flagellata, where Drysdale and Dallinger have shewn that an individual enclosed within a structureless cyst may divide first into two, then into four, and so on.
The process of budding differs mainly from that of simple fission in the fact that the two organisms produced are dissimilar in size, and also that the separation of the smaller organism from the larger is preceded by a process of growth in the latter, so that in the separation of the bud no essential part of the parent form is removed. This mode of reproduction is found amongst the Infusoria, Acineta, &c. An interesting variation in it is the internal gemmation of many of the Acineta, where a portion of the internal protoplasm with part of the nucleus is separated off to form a fresh individual. This mode of gemmation is connected by a series of gradations with the normal external gemmation. The organisms produced by gemmation are not always similar at birth to the parent; e.g. Acineta.
Both fission and gemmation when incomplete lead to the formation of colonies.
The third mode of reproduction, by spore formation, does not essentially differ from that by multiple fission. It consists in the breaking up of the organisms into a number (usually very considerable) of portions; each of which eventually develops into an organism like the parent form. All gradations between a simultaneous division of the organism into such spores and simple multiple fission are to be found, but this process of reproduction may be sometimes distinguished from that by such fission by the fact that the two processes may coexist in a single form, e.g. the biflagellate monad of Drysdale and Dallinger. In the majority of cases the spores produced differ at first from the parent organism not only in size but in other points, such as the possession of a flagellum, etc. They may even be without a nucleus when the parent organism is nucleated, as in the Gregarinidæ.
The encystment, which in many cases precedes reproduction by any of the above processes, and more especially by spores, is not an essential condition of their occurrence; and is probably in the first instance a protective arrangement which has become secondarily adapted to and connected with reproduction.
As has been already stated, all the above modes of reproduction take place in some of the Protozoa without any anterior process which can be regarded as of a sexual nature; but very often they are preceded by the temporary or permanent fusion of two or more individuals, such fusion being known as conjugation.
In most cases reproduction by spores is the consequence of conjugation, but in the Infusoria etc. where the fusion at conjugation is temporary (except Vorticella), there is probably merely a renewed activity--a rejuvenescence--which most likely results in active fission or budding. In the Gregarinidæ reproduction by spores usually follows conjugation, but may also take place without it. In some Flagellata reproduction by spores follows the conjugation of two individuals in a different stage of development. Thus in the springing Monad, described by Drysdale and Dallinger, a form produced by the fission of a monad in an amoeboid condition fuses with an ordinary monad to produce an individual, which then breaks up into spores. Another instance of the fusion of dissimilar individuals is afforded by Vorticella, where a free-swimming individual conjugates and is permanently united with a fixed one (Engelmann, Bütschli). Conjugation often consists in the fusion of more than two individuals. In conjugation where the fusion is permanent, the nuclei of the conjugating forms usually unite before the product breaks up into spores and where temporary fusion occurs in the Infusoria a division of the paranuclei and often of the nuclei takes place, followed by the ejection of parts of them, and a reproduction of new paranuclei and nuclei from the remainder of the original structures.
In order to understand the meaning of conjugation in connection with reproduction, it is important to understand how the two became in the first instance related. For the solution of this question the fact that many Protozoa have the capacity of temporarily or permanently fusing together without an immediate act of reproduction is of great importance. A good example of such fusion is supplied by Actinophrys. We must suppose in fact that the simple coalescence of two or more individuals gives a sufficient amount of extra vigour to their product, to compensate the race for the loss in number of individuals so caused. This extra vigour probably first exhibited itself especially by increased activity in reproduction, till finally the two processes, viz. that of conjugation and that of reproduction, came to be inseparably connected together.
The reproduction of the forms above the Protozoa, which are known as the Metazoa, takes place by two methods, viz. a sexual and an asexual one. The sexual process, which occurs in every known Metazoon[5], consists essentially, as is shewn in the second chapter of this work, in the fusion of two cells budded off from the parent organism, viz. the female cell or ovum, and the male cell or spermatozoon, and of the subsequent division of the compound cell so produced into a number of parts which build themselves up into an organism resembling one of the parents. The sexual process has obviously at first sight a very close resemblance to the process of conjugation. Since it is a question of fundamental importance to determine how sexual reproduction originated, it becomes necessary to examine how far this apparent resemblance is a real one, and how far sexual reproduction can be derived from reproduction following upon conjugation.
[5] Dicyema, if it is a true Metazoon, would seem to form an exception to this rule.
In spite of the general similarity between the two processes there is an obvious difficulty in comparing them, in that the result of conjugation is usually the breaking up of the individual formed by the fusion of two other individuals into a number of new organisms, while the result of the fusion which takes place in sexual reproduction is the formation of a single new organism. This difference between the two processes, great as it is, is perhaps apparent rather than real. It must be remembered that a single individual Metazoon is equivalent to a number of Protozoa coalesced to form a single organism in a higher state of aggregation. It results from this that the segmentation of the ovum which follows the sexual act may be compared to the breaking up of the product of conjugation into spores, the difference between the two processes consisting in the fact that in the one case the spores separate each to form an independent organism, while in the other they remain united and give rise to a single compound organism.
If the above considerations are well founded it seems permissible to accept the general view according to which sexual reproduction is derived from conjugation. It is necessary to suppose that, in a colony of Protozoa in the course of becoming a Metazoon, the capacity of reproduction by spores became localized in certain definite cells, and although the formation of spores from these cells may have been possible without previous conjugation, yet that conjugation gradually became established as the rule. The differentiation of primitively similar conjugating cells into male and female cells was probably a very early occurrence, since indications of an analogous differentiation, as has already been mentioned, are found in certain existing Protozoa (Monads, Vorticella, etc.). I have attempted to shew in the second chapter that the breaking up of the cell into spores without previous conjugation is perhaps provided against in the extrusion of the so-called 'directive body'.
With the differentiation of special germinal cells, to take the place of the whole individual in the act of conjugation, the possibility of each act of conjugation resulting in the production of only a single organism became introduced. Germinal cells can be indefinitely produced, and the reproductive capacity of a single individual is therefore unlimited; while if two whole individuals conjugated and only produced one from the process, the result would be a diminution instead of an increase in the race[6].
[6] In the vegetable kingdom there are numerous types of Thallophytes, which throw a considerable amount of light on the relation between sexual reproduction and conjugation. Subjoined are a few of the more striking cases. In Pandorina at the time of sexual reproduction the cells which constitute a colony divide each into sixteen, and the products of their division are set free. Pairs of them then conjugate and permanently fuse. After a resting stage the protoplasm is set free from its envelope after division into two or four parts. Each of these then divides into sixteen coherent cells and constitutes a new Pandorina colony. In OEdogonium the fertilization is effected by a spermatozoon fusing with an oosphere (ovum). The fertilized oosphere (oospore) then undergoes segmentation like the ovum of an animal; but the segments, instead of uniting to form a single organism, separate from each other, and each of them gives rise to a fresh individual (swarm-spore) which grows into a perfect OEdogonium. In Coleochæte the impregnation and segmentation take place nearly as in OEdogonium, but the segments remain united together, acquire definite cell walls, and form a single embryo. There is in fact in Coleochæte a true sexual reproduction of the ordinary type. (Vide S. H. Vines "On alternation of generation in the Thallophytes." Journal of Botany, Nov., 1879.)
It must be admitted that, in the present state of our knowledge, the passage from reproduction by spores following conjugation, to true sexual reproduction, can only be traced in a very speculative manner, and that a further advance in our knowledge may prove that the steps which I have attempted to sketch out are far from representing the true origin of sexual differentiation. The peculiar conjugation and fusion of two individuals to form Diplozoon paradoxum may be alluded to in this connection. This fusion merely results in the attainment of sexual maturity by the two conjugating individuals. It does not appear to me probable that this conjugation is in any way connected with the conjugation of the Protozoa, but the reverse must be borne in mind as a possibility.
It is not easy to decide whether the hermaphrodite or the dioecious state is the primitive one, or in other words whether the two conjugating cells, from which I have supposed the sexual products to originate, were derived in the first instance from one or from two colonies of Protozoa. On purely à priori grounds it seems probable that they were originally formed in one colony, and that their derivation from two colonies or individuals was inaugurated when the spermatozoon became motile. There can be no doubt that the dioecious state is a very early one, and that the majority of existing cases of hermaphroditism are secondary.
The above considerations with reference to the male and female cells appear to indicate that they were primitively homodynamous; a conclusion which is on the whole borne out by the history of their development.
Although the modes of reproduction amongst the Metazoa have been divided into the classes sexual and asexual, there is nevertheless one mode of asexual reproduction which ought to be classified with the sexual rather than with the asexual modes. I mean parthenogenesis, which consists essentially in the development of the ovum into a fresh individual without previous coalescence with the male element. This mode of reproduction, which has a very limited range in the animal kingdom, being confined to the Arthropoda and Rotifera, is undoubtedly secondarily derived from sexual reproduction. The conditions of its occurrence are discussed in the second chapter.
It is remarkable that in certain cases the absence of fertilization causes the production of males (Bees, a Saw-fly, Nematus ventricosus, etc.); more usually it results in the production of females only, and there are very often in the Arthropoda a series of successive generations of females all producing ova which develop parthenogenetically into females; eventually however, usually in direct or indirect connection with a change of food or temperature, or other conditions, ova are formed which give rise without fertilization both to males and females.
The true asexual modes of reproduction amongst the Metazoa consist of fission and gemmation. Gemmation is by far the most widely disseminated of the two. Various as are the methods in which it takes place, it seems nevertheless that cells derived from all the germinal layers, and very frequently from all the important organs of the adult, assist in forming the bud. Into the details of the process, which require in many points a fuller elucidation, it is not my purpose to enter.
Gemmation is a far commoner occurrence amongst the simpler than amongst the more highly organised forms. It appears to have been superadded to the sexual mode of reproduction quite independently in a number of different instances.
While there is no difficulty in understanding how gemmation may have started in such simple types as the Coelenterata, the manner in which it first originated in certain highly organised forms, as for instance the Ascidians, is somewhat obscure, but it seems probable that it began with the division of the developing germ into two or more embryos, at a very early stage of growth.
Such a division of the germ is, as has been shewn by Kleinenberg, normal in Lumbricus trapezoides[7] and Haeckel has shewn that an artificial division of the germ in the Siphonophora leads to the development of two individuals. It has been pointed out by various naturalists that the production of double monsters is often a phenomenon of the same nature. While it is next to impossible to understand how production of a bud could commence for the first time in the adult of a highly organised form, it is not difficult to form a picture of the steps by which the fission of the germ might eventually lead to the formation of buds in the adult state.
[7] The case of Pyrosoma, which might be cited in this connection, is probably secondary.
The coexistence of sexual reproduction with normal asexual multiplication, or with parthenogenesis, has led to a remarkable phenomenon in the animal kingdom known as alternations of generations[8].
[8] For an excellent account of this subject, vide Allen Thompson's article Ovum in Todd's Cyclopædia. The metamorphosis of the Echinoderms included under this head in Thompson's article is now known not to be a proper case of alternations of generations.
For the details of the various types of alternations of generations, and their origin, the reader is referred to the body of the work; but a few general remarks on the nature and origin of the process, and on its nomenclature, may conveniently be introduced in this place. The simplest cases are those in which an individual which produces by sexual means gives origin to asexual individuals differently organised to itself, which produce by budding the original sexual form, and so complete a cycle. Instances of this kind are supplied by the Hydrozoa, Annelida and Tunicata. In the case of the Tunicata (Doliolum) two different asexual generations may be interpolated between the sexual generations. In all these cases the origin of the phenomenon is easily understood. It appears, as is most clearly shewn in the case of the Annelida, that the ancestors of the species which now exhibit alternations of generations originally reproduced themselves at the same time both sexually and by budding, though probably the two modes of reproduction did not take place at the same season. Gradually a differentiation became established, by which sexual reproduction was confined to certain individuals, which in most instances did not also reproduce asexually. After the two modes of reproduction became confined to separate individuals, the dissimilarity in habits of life necessitated by their diverse functions caused a difference in their organization; and thus a complete alternation of generations became established. The above is no merely speculative history, since all gradations between complete alternations of generations and simple budding combined with sexual reproduction can be traced in actually existing forms.
The alternation of generations as it is found amongst the Entoparasitic Trematodes and most Cestodes, is to be explained in a slightly different way.
It appears that in these parasitic forms a complicated metamorphosis first arose from the parasite having to accommodate itself to the different hosts it was compelled to inhabit, owing to the liability of its primitive and subsequent hosts to be devoured[9]. A capacity for asexual multiplication--obviously of immense advantage to a parasite--appears to have been acquired in some of the stages of this metamorphosis, and an alternation of generations thus established.
[9] The appearance of Vertebrata on the globe as the forms which most frequently preyed on Invertebrate forms, and were themselves not so liable to be devoured, has no doubt had a great influence on the metamorphosis of internal parasites, and has amongst other things resulted in these parasites usually reaching their sexual state in a vertebrate host.
A nearly parallel series to that exhibiting alternations of sexual generations with generations which produce by budding is supplied by the cases where sexual generations alternate with parthenogenetic ones, or in some instances even with larvæ which reproduce sexually or else parthenogenetically.
The best known examples of this form of alternations of generations are found amongst the Insecta[10]. A simple case is that of the Aphides. The ova deposited by impregnated females give rise to forms differently organised to the parents but provided with an ovary[11]. The eggs from the ovary develop parthenogenetically within the oviduct, and so long as there is plenty of food and warmth the generations produced are always parthenogenetic forms. The failure of warmth and nutriment causes the production of true males and females, and so the cycle is completed. We must suppose that the capacity possessed by so many female insects of producing eggs capable of developing without the influence of the male element, has been, so to speak, taken hold of by natural selection, and has led to the production of viviparous parthenogenetic forms, by which, so long as food is abundant, a clear economy in reproduction is effected. The continuance of the species during winter is secured by the production of males and females, the females laying eggs in autumn which are hatched in the spring.
[10] For details vide Chapter on Insecta.
[11] The distinction drawn by Huxley between ova and pseudova does not appear to me a convenient one in practice.
In Chermes there is less modification of the primitive condition in that the parthenogenetic generations lay their eggs like the impregnated females. In the gall-flies (Cynipidæ), there is frequently an alternation of generations of the same kind as in Chermes; there being no viviparous forms. The individuals of the different generations differ from each other to some extent in all these cases.
A second type of alternations of parthenogenetic and sexual generations is exemplified by the cases of Chironomus and Cecidomyia, where the larvæ which develop from the eggs of the fertilized female produce parthenogenetically, by means of true ova, forms which eventually after several generations (Cecidomyia) of larval reproduction give rise to sexual forms. The explanation is here practically the same as in the case of Aphis, and is paralleled in the gemmiparous series by the production of buds in the larval forms of Trematodes, etc. A very similar occurrence takes place in Ascaris nigrovenosa (vide chapter on Nematoidea), except that larval forms, which carry on reproduction and then perish without developing farther, do so by a true sexual process. Thus there is an alternation of generations of adult and larval sexual forms. The Axolotl is an intermittent example of the same phenomenon.
As might be anticipated from the mode in which alternations of generations have become established, incomplete approximations to it are not uncommon. Such approximations are especially found in the Arthropoda, where alternations of sexual and parthenogenetic generations frequently take place, in which the individuals of different generations are similarly organised (Psychidæ, Apus, &c.). Another approximation is afforded by the parthenogenetic winter eggs of Leptodora amongst the Phyllopods, which give rise to Nauplius larvæ, while the young hatched from the summer eggs do not pass through a metamorphosis. Numerous transitional cases are also found amongst the forms in which there is an alternation of sexual and gemmiparous generations.
The whole of the cases to which allusion has been made in this section may be conveniently classed under the term alternations of generations, but the cases of alternation of two sexual generations, and of sexual and parthenogenetic generations, are classified by Leuckart, Claus, etc. as cases of heterogeny, which they oppose to the other form of alternation of generations. If special terms are to be adopted for the two kinds of alternation of generations, it would be perhaps convenient to classify the cases of alternations of sexual and gemmiparous generations under the term metagenesis, and to employ the term heterogamy for the cases of alternation of sexual and parthenogenetic generations.
The term Nurse (German Amme), employed for the asexual generations in metagenesis, may advantageously be dropped altogether.
I. THE OVUM AND SPERMATOZOON
THE OVUM.
The complete developmental history of any being constitutes a cycle. It is therefore permissible in treating of this history to begin at any point. As a matter of convenience the ovum appears to be the most suitable point of departure. The question as to the germinal layer from which it is ultimately derived is dealt with in a subsequent part of the work; the present chapter deals with its origin and growth.
General History of the Ovum.
Every young ovum (fig. 1) has the character of a simple cell. It is formed of a mass of naked protoplasm (a), containing in its interior a nucleus (b), within which there is a nucleolus (c). The nucleus and nucleolus are usually known as the germinal vesicle and germinal spot.
[FIG. 1. DIAGRAM OF THE OVUM. (From Gegenbaur.)
a. Granular protoplasm. b. Nucleus (germinal vesicle). c. Nucleolus (germinal spot).]
The ovum so constituted is developed either (1) from one cell out of an aggregation or layer of cells all of which have the capacity of becoming ova; or (2) from one of a number of cells segmented off from a polynuclear mass of protoplasm, not divided into separate cells. In both cases the cells which have the capacity of becoming ova may be spoken of as germinal cells, and in the case where the ova are ultimately developed from a polynuclear mass of protoplasm the latter structure may be called a germogen.
In some cases the whole of the germinal cells eventually become ova, but as a rule only a small proportion of them have this fate, the remainder undergoing various changes to be spoken of in the sequel.
Extended investigations have shewn that the distinction between germinal cells which are independent cells from the first, or derived from a germogen in which the nucleated protoplasm is not divided into cells, is an unimportant one; and closely allied forms may differ in this respect. It is moreover probable that a germogen of nucleated protoplasm is less common than is often supposed: it being a matter of great difficulty to determine the structure of the organs usually so described. A germogen is stated to be found in most Platyelminthes, Nematoidea, Discophora, Insecta, and Crustacea.
A more important distinction in the origin of the germinal cells is that afforded by their position. In this respect three groups may be distinguished. (1) The germinal cells may form the lining of a sack or tube, having the form of a syncytium or of an epithelium of separate cells (Platyelminthes, Mollusca, Rotifera, Echinodermata, Nematoidea, Arthropoda). (2) Or they may form a specialized part of the epithelium lining the general body cavity (Chætopoda, Gephyrea, Vertebrata). (3) Or they may form a mass placed between the two elsewhere contiguous primitive germinal layers (Coelenterata[12]).
[12] In all the Metazoa the generative organs are placed between the primitive germinal layers; and the peculiarity of their position in the Coelenterata depends on the absence of a body cavity and of a distinct mesoblast.
Types of transition between the first and second group are not uncommon. Such types, properly belonging to the second group, originate by a special membranous sack continuous with the oviduct being formed round the primitively free patch of germinal cells. Examples of this are afforded by the Discophora, the Teleostei, etc. It is very probable that all the cases which fall under the first heading may have been derived from types which belonged to the second group.
The mode of conversion of the germinal cells into ova is somewhat diverse. Before the change takes place the germinal cells frequently multiply by division. The change itself usually involves a considerable enlargement of the germinal cell, and generally a change in the character of the germinal vesicle, which in most young ova (fig. 2) is very large as compared to the body of the ovum. The most complicated history of this kind is that of the ovum of the Craniata. (Vide pp. 56, 57.)
[FIG. 2. OVUM OF CARMARINA (GERYONIA) HASTATA. (Copied from Haeckel.)
gd. Body of ovum. gv. Germinal vesicle. gm. Germinal spot.]
The ovum in its young condition is obviously nothing but a simple cell; and such it remains till the period when it attains maturity.
Nevertheless the changes which it undergoes in the course of its growth are of a very peculiar kind, and, consisting as they do in many instances of the absorption of other cells, have led various biologists to hold that the ovum is a compound structure. It becomes therefore necessary to consider the processes by which the growth and nutrition of the ovum is effected before dealing with the structure of the ovum at all periods of its history.
[FIG. 3. FEMALE GONOPHORE OF TUBULARIA MESEMBRYANTHEMUM. CONTAINING ONE LARGE OVUM (ov) AND A NUMBER OF GERMINAL CELLS (g.c.).
ep. Epiblast (Ectoderm). hy. Hypoblast (Entoderm). ov. Ovum. g.c. Germinal cells.]
The ovum is of course nourished like every other cell by the nutritive fluids in which it is surrounded, and special provisions are made for this, in that the ovary is very frequently placed in contiguity with vascular channels. But in addition to such nutrition a further nutrition, the details of which are given in the special part of this chapter, is provided for in the germinal cells which do not become ova.
In the simplest case, as in many Hydrozoa (fig. 3), the germinal cells which do become ova are assimilated by the ovum much in the manner of an Amoeba.
In other cases the ovum becomes invested by a special layer of cells, which then constitutes what is known as a follicle. The cells which form the follicle are often germinal cells, e.g. Holothuria, Insecta (fig. 17), Vertebrata (fig. 19). In other cases they seem rather to be adjoining connective-tissue or epithelioid cells, though it is sometimes difficult to draw the line between such cells and germinal cells. Examples of follicles formed of ordinary connective-tissue cells, are supplied by Asterias, Bonellia (fig. 16), Cephalopoda (fig. 14), etc.
A membrane enclosing the ovum without a lining of cells, as in many Arachnida, vide p. 51, has no true analogy with a follicle and does not deserve the same name.
The function of the follicle cells appears to be, to elaborate nutriment for the growth of the ovum. The follicle cells are not as a rule directly absorbed into the body of the ovum, though in some instances, as in Sepia (vide p. 40), they are eventually assimilated in this way.
In many cases some of the germinal cells form a follicle, while other germinal cells form a mass within the follicle destined eventually to be used as pabulum. Insects supply the best known examples of this, but Piscicola, Bonellia (?) may also be cited as examples of the same character. In the Craniata (pp. 56-58) some of the germinal cells which advance a certain distance on the road towards becoming ova, are eventually used as pabulum, before the formation of the follicle; while other germinal cells form at a later period the follicular epithelium. A peculiar case is that of the Platyelminthes (fig. 9), where a kind of follicle is constituted by the cells of a specially differentiated part of the ovary, known as the yolk-gland. The cells of this follicle may either remain distinct, and continue to surround the ovum after its development has commenced, and so be used as food by the embryo; or they may secrete yolk particles, which enter directly into the protoplasm of the ovum.
For further variations in the mode of nutrition the reader is referred to the special part of this chapter. Suffice it to say that none of the known modes of nutrition indicate that the ovum becomes a compound body any more than the fact of an Amoeba feeding on another Amoeba would imply that the first Amoeba ceased thereby to be a unicellular organism.
The constitution of the ovum may be considered under three heads:--
(1) The body of the ovum. (2) The nucleus or germinal vesicle. (3) The investing membranes.
The body of the ovum. The essential constituent of the body of the ovum is an active living protoplasm. As a rule there are present certain extraneous matters in addition, which have not the vital properties of protoplasm. The most important of these is known as food-yolk, which appears to be generally composed of an albuminoid matter.
The body of the ovum is at first very small compared with the germinal vesicle, but continually increases as the ovum approaches towards maturity. It is at first comparatively free from food-yolk; but, except in the rare instances where it is almost absent, food-yolk becomes deposited in the form of granules, or highly refracting spheres, by the inherent activity of the protoplasm during the later stages in the ripening of the ovum. In many instances the protoplasm of the ovum assumes a sponge-like or reticulate arrangement, a fluid yolk substance being placed in the meshes of the reticulum. The character of the food-yolk varies greatly. Many of its chief modifications are described below. There is not unfrequently present in the vitellus a peculiar body known as the yolk nucleus, which is very possibly connected with the formation of the food-yolk. It is found in many Arachnida, Myriapoda, Amphibia, etc.[13]
[13] For details on the yolk nucleus vide Balbiani, Leçons s. l. Génération d. Vertébrés. Paris, 1879. In this work the author maintains very peculiar views on the nature and function of the yolk nucleus, which do not appear to me well founded.
[FIG. 4. A. OVUM OF HYDRA IN THE AMOEBOID STATE, WITH YOLK-SPHERULES (PSEUDOCELLS) AND CHLOROPHYLL GRANULES. (After Kleinenberg.)
gv. Germinal vesicle.
B. SINGLE PSEUDOCELL OF HYDRA.]
More important for the subsequent development than the variation in the character of the food-yolk is its amount and distribution. In a large number of forms it is distributed unsymmetrically, the yolk being especially concentrated at one pole of the ovum, the germinal vesicle, surrounded by a special layer of protoplasm comparatively free from food-yolk, being placed at the opposite pole. In the Arthropoda it has in most instances a symmetrical distribution. Further details on this subject are given in connection with the segmentation; the character of which is greatly influenced by the distribution of food-yolk.
The body of the ovum is usually spherical, but during a period in its development it not unfrequently exhibits a very irregular amoeboid form, e.g. Hydra (fig. 4), Halisarca.
[FIG. 5. UNRIPE OVUM OF TOXOPNEUSTES LIVIDUS. (Copied from Hertwig.)]
The germinal vesicle. The germinal vesicle exhibits all the essential characters of a nucleus. It has a more or less spherical shape, and is enveloped by a distinct membrane which seems, however, in the living state to be very often of a viscous semi-fluid nature and only to be hardened into a membrane by the action of reagents (Fol). The contents of the germinal vesicle are for the most part fluid, but may be more or less granular. Their most characteristic components are, however, a protoplasmic network and the germinal spots[14]. The protoplasmic network stretches from the germinal spots to the investing membrane, but is especially concentrated round the former. (Fig. 5.) The germinal spot forms a nearly homogeneous body, with frequently one or more vacuoles. It often occupies an eccentric position within the germinal vesicle, and is usually rendered very conspicuous by its high refrangibility. In many instances it has been shewn to be capable of amoeboid movements (Hertwig, Eimer), and is moreover more solid and more strongly tinged by colouring reagents than the remaining constituents of the germinal vesicle.
[14] In the germinal vesicles of very young ova the reticulum is often absent.
In many instances there is only one germinal spot, or else one main spot and two or three accessory smaller spots. In other cases, e.g. Osseous Fishes, Echinaster fallax, Eucope polystyla, there are a large number of nearly equal germinal spots which appear to result from the division or endogenous proliferation of the original spot. Sometimes the germinal spots are placed immediately within the membrane of the germinal vesicle (Elasmobranchii and Sagitta). In many Lamellibranchiata, in the earthworm, and in many Chætopoda the components of the germinal spot become separated into two nearly spherical masses (fig. 12), which remain in contiguity along a small part of their circumference, and are firmly united together. The smaller of the two parts is more highly refractive than the larger. Hertwig has shewn that the germinal spot is often composed of two constituents as in the above cases, but that the more highly refractive material is generally completely enclosed by the less dense substance. By Fol the germinal spot is stated to be absent in a species of Sagitta, but this must be regarded as doubtful. In young ova the relative size of the germinal vesicle is very considerable. It occupies in the first instance a central position in the ovum, but at maturity is almost always found in close proximity to the surface. Its change of position in a large number of instances is accomplished during the growth of the ovum in the ovary, but in other cases does not take place till the ovum has been laid.
As the ovum attains maturity, important changes take place in the constitution of the germinal vesicle, which are described in the next chapter.
The egg membranes. A certain number of ova when ready to be fertilized are naked cells devoid of any form of protecting covering, but as a rule the ovum is invested by some form of membrane. Such coverings present great variety in their character and origin, and may be conveniently (Ludwig, No. 4) divided into two great groups, viz. (1) those derived from the protoplasm of the ovum itself or from its follicle, which may be called primary egg membranes; and (2) those formed by the wall of the oviduct or otherwise, such as the egg-shell of a bird, which may be called secondary egg membranes.
[FIG. 6. OVUM OF TOXOPNEUSTES VARIEGATUS WITH THE PSEUDOPODIA-LIKE PROCESSES OF THE PROTOPLASM PENETRATING THE ZONA RADIATA (zr). (After Selenka.)]
The primary egg membranes may again be divided into two groups (Ed. van Beneden, No. 1), viz., (1) those formed by the protoplasm of the ovum, to which the name vitelline membranes will be applied; and (2) those formed by the cells of the follicle, to which the name chorion will be applied.
The secondary egg membranes will be dealt with in connection with the systematic account of the development of the various groups. They coexist as a rule with primary membranes, though in some types (Cephalophorous Mollusca, many Platyelminthes, etc.), they constitute the only protecting coverings of the ovum.
The vitelline membranes are either simple structureless membranes or present numerous radial pores. Membranes with the latter structure are very widely distributed, Echinodermata, Gephyrea, Vertebrata, etc. (Vide figs. 5 and 7.) The function of the pores appears to be a nutritive one. They either serve for the emission of pseudopodia-like processes of the protoplasm of the ovum, as has been very beautifully shown in the case of Toxopneustes by Selenka (fig. 6), or they admit (?) processes of the follicular epithelial cells (Vertebrata). Their presence is in fact probably caused by the existence of such processes, which prevent the continuous deposition of the membrane. The term zona radiata will be applied to perforated membranes of this kind. Two vitelline membranes, one perforated and the other homogeneous, may coexist at the same time, e.g. Sipunculida, Vertebrata. (Fig. 7.)
[FIG. 7. SECTION THROUGH A SMALL PART OF THE SURFACE OF AN OVUM OF AN IMMATURE FEMALE OF SCYLLIUM CANICULA.
fe. Follicular epithelium. vt. Vitelline membrane. Zn. Zona radiata. yk. Yolk with protoplasmic network.]
The chorion is often ornamented with various processes, etc. It is in many cases doubtful whether a particular membrane is a chorion or a vitelline membrane.
All the membranes which surround the ovum may be provided with a special aperture known as the micropyle. A micropyle is by no means found in the majority of types, and there is no homology between the various apertures so named. Micropyles have two functions, either (1) to assist in the nutrition of the ovum during its development, or (2) to permit the entrance of the spermatozoa. The two functions may in some cases coexist. Micropyles of the first class are developed at the point of attachment of the ovum to the wall of the ovary or to its follicle. Good examples of this kind of micropyle are afforded by the Lamellibranchiata (fig. 12), Holothuria, and many Annelida (Polynoe, etc.). The micropyle of the Lamellibranchiata (p. 37) probably serves also to admit the spermatozoa. The second type of micropyle is found in many Insecta, Teleostei, etc.
GENERAL BIBLIOGRAPHY OF THE OVUM.
(1) Ed. van Beneden. "Recherches sur la composition et la signification de l'oeuf," etc. Mém. cour. d. l'Acad. roy. des Sciences de Belgique, Vol. XXXIV. 1870.
(2) R. Leuckart. Artikel "Zeugung," R. Wagner's Handwörterbuch d. Physiologie, Vol. IV. 1853.
(3) Fr. Leydig. "Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer Bedeutung." Oken, Isis, 1848.
(4) Ludwig. "Ueber d. Eibildung im Thierreiche." Arbeiten a. d. zool.-zoot. Institut Würzburg, Vol. I. 1874[15].
(5) Allen Thomson. Article "Ovum" in Todd's Cyclopædia of Anatomy and Physiology, Vol. V. 1859.
(6) W. Waldeyer. Eierstock u. Ei. Leipzig, 1870.
[15] A very complete and critical account of the literature is contained in this paper.
Special History of the Ovum in different types.
COELENTERATA.
(7) Ed. van Beneden. "De la distinction originelle d. testicule et de l'ovaire." Bull. Acad. roy. Belgique, 3e série, Vol. XXXVII. 1874.
(8) R. and O. Hertwig. Der Organismus d. Medusen. Jena, 1878.
(9) N. Kleinenberg. Hydra. Leipzig, 1872.
Amongst the Coelenterata the ova are developed in imperfectly specialized organs, which are situated in various parts of the body, for the most part in the space between the epiblast and the hypoblast.
In Hydra the locality where the ova are developed only becomes specialized at the time when an ovum is about to be formed. At one or more points the interstitial cells of the epiblast increase in number and form a protuberance of germinal cells, which may be called the ovary. In this ovary a single ovum is formed by the special growth of one cell. (Kleinenberg, No. 9.) In the free and attached gonophores of Hydrozoa, the ova appear either around the walls of the stomach, or the radial canals, or around other parts of the gastro-vascular canals.
[FIG. 8. RIPE OVUM OF EPIBULIA AURANTIACA. THE GERMINAL VESICLE HAS BECOME INVISIBLE WITHOUT REAGENTS.
Copied from Metschnikoff, "Entwicklung der Siphonophoren." Zeitschrift f. wiss. Zool., Vol. XXIV. 1874.
p.d. Peripheral layer of denser protoplasm. p.m. Central area consisting of a protoplasmic meshwork.]
Their close relations to the gastrovascular canals are probably determined by the greater nutritive facilities thereby afforded. (Hertwig, No. 8.)
In the permanent Medusa forms the ova have similar relations to the gastro-vascular system. Amongst the Actinozoa the ova are usually developed between the epiblast and the hypoblast in the walls of the gastric mesenteries. Amongst the Ctenophora the ova are situated in close relation with the peripheral canals of the gastro-vascular system, which run along the bases of the ciliated bands. There are many examples amongst the Coelenterata of ova which retain in their mature state the very simple constitution which has been described as characteristic of all young ova; and which are, when laid, absolutely without any trace of a vitelline membrane or chorion. In many other cases both amongst the Medusæ, the Siphonophora, and the Ctenophora, the ripe egg exhibits a distinction into two parts. The outer part is composed of a dense protoplasm, while the interior is composed of a network or more properly a spongework of protoplasm enclosing in its meshes a more fluid substance. (Fig. 8.)
In some cases the ovum while still retaining the constitution last described becomes invested by a very delicate membrane. Such is the constitution of the ripe ovum of Hippopodius gleba amongst the Siphonophora[16] and of the eggs of Geryonia amongst the permanent Medusæ[17]. The ripe eggs of the Ctenophora usually present a similar structure[18]. After being laid they are found to be invested by a delicate membrane separated by a space filled with fluid from the body of the ovum. The latter is composed of two layers, an outer one of finely granular protoplasm and an inner layer consisting of a protoplasmic spongework containing in its meshes irregular spheres. These latter are stated by Agassiz to be of a fatty nature, and it is probable that in most cases where a protoplasmic network is present, this alone constitutes the active protoplasm and that the substance which fills up its meshes is to be looked on as a form of food-yolk or deutoplasm, though it appears sometimes to have the power of assimilating the firmer yolk particles.
[16] Metschnikoff. Zeitschrift f. wiss. Zoologie, Vol. XXIV. 1874.
[17] Herman Fol. Jenaische Zeitschrift, Vol. VII.
[18] Kowalevsky. "Entwicklungsgeschichte d. Rippenquallen." Mémoire de l'Acad. Pétersbourg, 1866. And Alex. Agassiz. "Embryology of the Ctenophoræ." Amer. Acad. of Science and Arts, Vol. X. No. 111.
The membrane which invests the ovum of many of the Coelenterata is probably a vitelline membrane.
The ova of the Hydrozoa take their origin, in most groups at any rate[19], from the deeper layer of the epiblast (interstitial layer of Kleinenberg). The interstitial cells in the ovarian region form primary germinal cells, and by an excess of nutrition certain of them outstrip their fellows and become young ova. Such ova differ from the full-grown ova already described, mainly in the fact that they have a proportionately smaller amount of protoplasm round the germinal vesicle. They grow to a considerable extent at the expense of germinal cells which do not become converted into ova.
[19] The view of van Beneden, according to which the ova have an endodermal (hypoblastic) origin, has been shewn to be at any rate confined to certain groups. The whole question of the origin of the generative products from the germinal layers in the Coelenterata is still involved in great obscurity.
The ova of many Coelenterata undergo changes of a more complicated kind before attaining their full development. Of these ova that of Hydra may be taken as the type. The ovary of Hydra (Kleinenberg, No. 9) is constituted of angular flattish germinal cells of which no single one can be at first distinguished from the remainder. As growth proceeds one of the cells occupying a central position becomes distinguished from the remaining cells by its greater size, and wedge-like shape. It constitutes the single ovum of the ovary. After it has become prominent it grows rapidly in size, and throws out irregular processes. The germinal vesicle, which for a considerable time remains unaltered, also at length begins to grow; and the sharply defined germinal spot which it contains after reaching a certain size completely vanishes. After the atrophy of the germinal spot, there appears in the middle of the ovum a number of roundish yolk granules.
The shape of the ovum becomes more irregular, and chlorophyll granules, in addition to the yolk granules, make their appearance in it. A fresh germinal spot of circular form also arises in the germinal vesicle. Protoplasmic processes are next thrown out in all directions, giving to the ovum a marvellous amoeboid character. (Fig. 4.) The amoeboid form of the ovum serves no doubt to give it a larger surface for nutrition. Coincidently with the assumption of an amoeboid form there appear in the ovum a great number of peculiar bodies. They are vesicles with a thick wall bearing a conical projection into the interior which is filled with fluid. (Fig. 4B.) These bodies are formed directly from the protoplasm of the ovum, and are to be compared both morphologically and physiologically with the yolk-spherules of such an ovum as that of the Bird. They are called pseudocells by Kleinenberg, and are found with slightly varying characters in many ova of the Hydrozoa.
They first appear as small highly refracting granules; in these a cavity is formed which is at first central but is eventually pushed to one side by the formation of a conical projection from the wall of the vesicle.
After the growth of the ovum is completed the amoeboid processes gradually withdraw themselves, and the ovum assumes a spherical form; still however continuing to be invested by the remaining cells of the ovary. It is important to notice that the egg of Hydra retains throughout its whole development the characters of a single cell, and that the pseudocells and other structures which make their appearance in it are not derived from without, and supply not the slightest ground for regarding the ovum as a structure compounded of more than one cell.
The development of the ova of the Tubularidæ, which has been supposed by many investigators to present very special peculiarities, takes place on essentially the same type as that of Hydra, but the germinal vesicle remains permanently very small and difficult to observe. The mode of nutrition of the ovum may be very instructively studied in this type. The process is one of actual feeding, much as an Amoeba might feed on other organisms. Adjoining one of the large ova of the ovary there may be seen a number of small germinal cells. (Fig. 3.) The boundary between these cells and the ovum is indistinct. Just beyond the edge of the ovum the small cells have begun to undergo retrogressive changes; while at a little distance from the ovum they are quite normal (g.c.)[20].
[20] The above description of the ova of the Tubularidæ is founded on sections of the gonophores of Tubularia mesembryanthemum. Dr Kleinenberg informs me however that the absence of a distinct boundary between the germinal cells and the ovum is not usual.
PLATYELMINTHES.
(10) P. Hallez. Contributions à l'Histoire naturelle des Turbellariés. Lille, 1879.
(11) S. Max Schultze. Beiträge z. Naturgeschichte d. Turbellarien. Greifswald, 1851.
(12) C. Th. von Siebold. "Helminthologische Beiträge." Müller's Archiv, 1836.
(13) C. Th. von Siebold. Lehrbuch d. vergleich. Anat. d. wirbellosen Thiere. Berlin, 1848.
(14) E. Zeller. "Weitere Beiträge z. Kenntniss d. Polystomen." Zeit. f. wiss. Zool., Bd. XXVII. 1876.
[Vide also Ed. van Beneden] (No. 1).
This group, under which I include the Trematodes, Cestodes, Turbellarians and Nemertines, has played an important part in all controversies relating to the nature and composition of the ovum. The peculiarity in the development of the ovum in most members of this group consists in the fact that two organs assist in forming what is usually spoken of as the ovum. One of these is known as the ovary proper, and the other as the vitellarium or yolk-gland. In the sequel the term ovum will be restricted to the product of the first of these organs. In Trematodes the ovary forms an unpaired organ directly continuous with an oviduct into which there open the ducts from paired yolk-glands.
The ovary has a sack-like form and contains in some instances a central lumen (Polystomum integerrimum). At the blind end of the organ is placed the germinal tissue. This part is, according to the accounts of the majority of investigators, formed of a polynuclear mass of protoplasm not divided into distinct cells. Whether it is really formed of undivided protoplasm or not, it is quite certain that a little lower down in the organ distinct cells are found, which have been segmented off from the above mass, and are formed of a large nucleus and nucleolus, surrounded by a delicate layer of protoplasm. These cells are the young ova. They usually assume a more or less angular form from mutual pressure, and, in the cases where the ovary has a lumen, constitute a kind of epithelial lining for the ovarian tube. They become successively larger in passing down the ovary, and, though in most cases naked, are in some instances (Polystomum integerrimum) invested by a delicate vitelline membrane. Eventually the ova pass into the oviduct and become free and at the same time assume a spherical form.
In the oviduct the ovum receives somewhat remarkable investing structures, derived from the organ before spoken of as the yolk-gland. The yolk-gland consists of a number of small vesicles, each provided with a special duct, connected with the main duct of the gland. Each vesicle is lined by an epithelium of cells provided with doubly contoured membranes, and containing nuclei.
As the yolk cells grow older refracting spherules become deposited in their protoplasm, which either completely hide the nucleus, or render it very difficult to see. In the majority of cases the entire cells forming the lining of the vesicles constitute the secretion of the yolk-gland. They invest the ovum, and around them is formed a shell or membrane. In some cases (e.g. Polystomum integerrimum) the yolk cells retain their cellular character and vitality till the embryo is far developed. In other cases they lose their membrane and nucleus shortly after the formation of the egg-shell, and break up into a fluid, holding in suspension a number of yolk granules. A partial disorganisation of the yolk cells can also take place before they surround the ovum; while in some species of Distomum they completely break up before leaving the yolk-gland.
[FIG. 9. GENERATIVE SYSTEM OF VORTEX VIRIDIS. (From Gegenbaur, after Max Schultze.)
t. Testis. v.d. Vasa differentia. v.s. Seminal vesicle. p. Penis. u. Uterus. o. Ovary. v. Vagina. g.v. Yolk-glands. r.s. Receptaculum seminis.]
There is thus a complete series of gradations between the investment of the ovum by a number of distinct cells, and its investment by a layer of fluid containing yolk-spherules in suspension. In neither the one case nor the other do the investing structures take any share in the direct formation of the embryo from the ovum. Physiologically speaking they play the same part as the white in the fowl's egg.
The egg-shell, which is usually formed by a secretion of a special shell-gland opening into the oviduct, exhibits one or two peculiarities in the different species of Trematodes. In Amphistomum subclavatum it presents at one extremity a thickened area, which is pierced by a narrow micropyle. In other cases one extremity of the egg-shell is produced into a long process, and sometimes even both extremities are armed in this way. Opercula and other types of armature are also found in different forms.
The mode of development of the ovum in Cestodes is very nearly the same as in Trematodes.
The ovum becomes enveloped in the usual secretion of the yolk-gland; and an egg-shell is always formed by the secretion of a special shell-gland.
Amongst the Turbellarians and Nemertines, there are greater variations in the arrangement of the female generative glands, than in the preceding types. In most of the Rhabdocoela and fresh-water Dendrocoela these organs resemble in their fundamental characters those of the Trematodes and Cestodes. There are present a paired or single ovary and a paired yolk-gland. The general arrangement of the organs is shewn in fig. 9.
The blind end of the ovaries is usually (Ed. van Beneden, etc.) stated to be formed of a polynuclear protoplasmic basis, but Hallez (No. 10) has recently insisted that, even at the extreme end of the ovary, the germinal cells are quite distinct, and not confounded together.
With one or two exceptions the yolk cells secreted by the vitellarium retain their vitality till they are swallowed by the embryo, after the development of its mouth. The few not so swallowed become disintegrated. They are granular nucleated cells, and, as was first shewn by von Siebold, are remarkable for exhibiting spontaneous amoeboid movements.
Very important light on the nature of the vitellarium is afforded by the structure of the generative organs in Prorhyncus and Macrostomum.
In Prorhyncus there is no separate vitellarium, but the lower part of the ovarian tube functionally and morphologically replaces it. The ovum becomes surrounded by yolk cells, which according to Hallez (No. 10) retain their vitality for a long time. According to Ed. van Beneden yolk-spherules are formed in the protoplasm of the ovum itself, in addition to and independently of the surrounding yolk cells. In Convoluta paradoxa a special vitellarium is stated to be absent; though a deposit of yolk is formed round the ovum (Claparède).
In Macrostomum again the yolk-glands are at most represented by a lower specialized part of the ovarian tube. The ova in passing down become filled with yolk-spherules. According to Ed. van Beneden these spherules are formed in the protoplasm of the ovum itself; but this is explicitly denied by Hallez, who finds that they are formed from the lining cells of the ovarian tube, which, instead of retaining their vitality as in Prorhyncus, break up and form a granular mass which is absorbed by the protoplasm of the ovum.
In Prostomum caledonicum (Ed. van Beneden) the generative organs are formed on the same plan as in other Rhabdocoela, but the cells which form the yolk-gland give rise to yolk particles which enter the ovum, instead of to a layer of yolk cells surrounding the ovum.
Amongst the marine dendrocoelous Turbellarians the ova are formed in separate sacks widely distributed in the parenchyma of the body between the alimentary diverticula. In these the ova undergo their complete development, without the intervention of yolk-glands.
The ovaries of the Nemertines more nearly resemble those of the marine Dendrocoela than those of the Rhabdocoela. They consist of a series of sacks situated on the two sides of the body between the prolongations of the digestive canal. The eggs are developed in these sacks in a perfectly normal manner, and in many cases become filled with yolk-spherules which arise as differentiations of the protoplasm of the ovum. The protecting membranes of the ova have not been accurately studied. In some cases[21] two membranes are present, an internal and an external. The former, immediately investing the vitellus, is very delicate: the external one is thicker and hyaline.
[21] Amphiporus lactiflorius and Nemertes gracilis. McIntosh. Monograph on British Nemertines. Ray Society.
The constitution of the female generative organs of the Trematodes was first clearly ascertained by von Siebold (No. 12). He originally, though not very confidently, propounded the view that the germinal vesicles alone were formed in the ovary and that the protoplasm of the ovum was supplied by the yolk-gland. This view has long been abandoned, and von Siebold (No. 13) himself was the first to recognize that true ova with a protoplasmic body containing a germinal vesicle and germinal spot were formed in the ovary. The Trematodes have however not ceased to play an important part in forming the current views upon the development of ova, and have quite recently served Ed. van Beneden as his type in exposing his general view upon this subject.
His view consists fundamentally in regarding the secretion of the yolk-glands, which in most cases merely invests the ovum, as homologous with the yolk-spherules which fill the protoplasm of many eggs; and he considers the part of the ovary where in most forms the ova receive their supply of yolk particles, as equivalent to the vitellarium of the Platyelminthes. He further appears to regard the primitive state as that exemplified in Trematodes, Cestodes, etc., and holds that the ovarian types characteristic of other forms are secondarily derived from this, by the coalescence of the primitively distinct vitellarium with the ovary proper.
This appears to me a case of putting the cart before the horse. To my mind the vitellarium is to be regarded, as has already been suggested by Gegenbaur, Hallez, etc. as a special differentiation of the primitively simple ovarian tube, and the instances Of Macrostomum and Prorhyncus just cited appear to me to indicate some of the steps in this differentiation. In Macrostomum the cells of the lower part of the oviduct simply supply a kind of nutriment to the ovum in the form of granular yolk particles, while in Prorhyncus the yolk cells of the lower part of the ovarian tube form a complete investment of independent cells for the ovum. If this lower part of the ovarian tube were to grow out as a special diverticulum we should have produced a normal vitellarium. But even with the above modification the theory of van Beneden appears to me not completely satisfactory. The view that the yolk-spherules are of the same nature as the yolk cells is mainly supported by the case of Prostomum caledonicum, where the vitellarium produces the yolk particles which fill the ovum. The cases Of Prorhyncus and Macrostomum give a different complexion to that of Prostomum caledonicum. From the first of these especially it appears that, even when normal yolk cells surround the ovum, yolk particles can be deposited independently in the protoplasm of the ovum.
The most probable view of the nature of the vitellarium is that of Gegenbaur, Hallez, etc., according to which it is to be regarded as a specially modified part of the ovarian tube. On this view the nature and function of the yolk cells admit of a fairly simple explanation. They are to be regarded as primary germinal cells like those in the ovaries of Hydra, Tubularia, etc., which do not become converted into ova. Like these cells they may in some instances, Macrostomum, Prostomum, etc., serve directly in the nutrition of the ovum. In other cases they retain their independence and serve for the late nutrition of the embryo. In both instances they retain the faculty, normally possessed by ova, of forming yolk particles in their protoplasm.
ECHINODERMATA.
(15) C. K. Hoffmann. "Zur Anatomie d. Echiniden u. Spatangen." Niederländisch. Archiv f. Zoologie, Vol. I. 1871.
(16) C. K. Hoffmann. "Zur Anatomie d. Asteriden." Niederländisch. Archiv f. Zoologie, Vol. II. 1873.
(17) H. Ludwig. "Beiträge zur Anat. d. Crinoiden." Zeit. f. wiss. Zool., Vol. XXVIII. 1877.
(18) Joh. Müller. "Ueber d. Canal in d. Eiern d. Holothurien." Müller's Archiv, 1854.
(19) C. Semper. Holothurien. Leipzig, 1868.
(20) E. Selenka. Befruchtung d. Eies v. Toxopneustes variegatus, 1878.
[Vide also Ludwig (No. 4), etc.]
The eggs of the Echinodermata present in their development certain points of interest.
The ovaries themselves are usually surrounded by a special vascular dilatation. In the Asteroidea, the Echinoidea, and the Holothuroidea the organs have the form of sacks; specially surrounded in the two former groups, and probably the latter, by a vascular sinus formed as a dilatation of one of the generative vessels. In the Crinoids they have the form of a hollow rachis completely surrounded by a blood-vessel. (Fig. 11, b.) The proximity of the ovaries (generative organs) to the vascular system in these forms has clearly the same physiological significance as the proximity of the ovaries (generative organs) to the radial vessels in the Coelenterata.
In the Asteroidea, the Echinoidea and the Holothuroidea the ovaries have the form of sacks lined by an epithelium of germinal cells, and the ova are formed by the enlargement of these cells, which, when they have reached a certain size, become detached from the walls, and fall into the cavity of the ovarian sack. In Toxopneustes (Selenka) and very probably in other forms only a few of the epithelial cells undergo conversion into ova: the remainder undergo repeated division, and, as in so many other cases, are eventually employed in the nutrition of the true ova. In the nearly ripe ova of Asterias Fol has described a flattened follicular epithelium the origin of which is unknown.
[FIG. 10. OVUM OF TOXOPNEUSTES VARIEGATUS WITH THE PSEUDOPODIA-LIKE PROJECTIONS OF THE PROTOPLASM PENETRATING THE ZONA RADIATA (zr). (After Selenka.)]
In Holothuria (Semper) a further differentiation of the germinal cells, not destined to become ova, takes place. They surround the enlarged cell which forms the true ovum, for which they constitute a kind of follicular capsule. This capsule is attached by a stalk to the walls of the ovary, and the ovum lies freely in it except for an area nearly opposite its (the capsule's) point of attachment, where the ovum adheres to the wall of the capsule. Subsequently the follicle cells which form the capsule fuse together, and form a definite membrane in which only the nuclei remain distinct. Within the membranous capsule there is formed for the ovum an albuminous zona radiata. At the point where the ovum is attached to its capsule this membrane cannot be developed, and therefore remains incomplete. The perforation so formed, becomes the micropyle of the Holothurian egg, which was first discovered by Joh. Müller. The albuminous membrane just described for Holothurians is also found in Asteroids (fig. 5) and Echinoids. In these groups there is no proper micropyle, though in Ophiothrix a nutritive passage perforates the membrane at the attachment of the ovum before the period when the ovum becomes free (Ludwig). The formation of the zona radiata has been studied by Selenka. It is secreted by the protoplasm of the ovum, and has a gelatinous consistency, and after it is formed the peripheral layer of the protoplasm of the ovum sends out through it pseudopodia-like processes to absorb nutriment from without. These processes are at first large and irregular, but soon become finer and finer (fig. 10), and acquire a regular radiating arrangement. They are withdrawn when the ovum is ripe, but they nevertheless give rise to the finely radiated appearance of the membrane, the radii being in reality delicate pores.
[FIG. 11. TRANSVERSE SECTION THROUGH THE PINNA OF A SEXUALLY MATURE COMATULA. (From Gegenbaur, after Ludwig.)
p. Tentacle. g. Lumen of genital rachis. w. Water-vascular vessel. n. Nerve cord. b. Blood-vessel on nerve cord and round genital rachis. cg. Genital canal. cd. Dorsal section of the body cavity. cv. Ventral section of body cavity.]
In the Crinoids the generative rachis consists of a tube, the epithelium of which is formed of the primary germinal cells. (Fig. 11.) While some of these cells enlarge and become ova, the remainder supply the elements for a follicular epithelium, which is established round the ova, exactly as in Holothurians.
MOLLUSCA.
Lamellibranchiata.
(21) H. Lacaze-Duthiers. "Organes génitaux des Acéphales Lamellibranches." Ann. Sci. Nat., 4me série, Vol. II. 1854.
(22) W. Flemming. "Ueb. d. er. Entwick. am Ei d. Teichmuschel." Archiv f. mikr. Anat., Vol. X. 1874.
(23) W. Flemming. "Studien üb. d. Entwick. d. Najaden." Sitz. d. k. Akad. Wiss. Wien, Vol. LXXI. 1875.
(24) Th. von Hessling. "Einige Bemerkungen, etc." Zeit. f. wiss. Zool., Bd. V. 1854.
(25) H. von Jhering. "Zur Kenntniss d. Eibildung bei d. Muscheln." Zeit. f. wiss. Zool., Vol. XXIX. 1877.
(26) Keber. De Introitu Spermatozoorum in ovula, etc. Königsberg, 1853.
(27) Fr. Leydig. "Kleinere Mittheilung etc." Müller's Archiv, 1854.
Gasteropoda.
(28) C. SEMPER. "Beiträge z. Anat. u. Physiol. d. Pulmonaten." Zeit. f. wiss. Zool., Vol. VIII. 1857.
(29) H. Eisig. "Beiträge z. Anat. u. Entwick. d. Pulmonaten." Zeit. f. wiss. Zool., Vol. XIX. 1869.
(30) Fr. Leydig. "Ueb. Paludina vivipara." Zeit. f. wiss. Zool., Vol. II. 1850.
Cephalopoda.
(31) AL. KÖLLIKER. Entwicklungsgeschichte d. Cephalopoden. Zurich, 1844.
(32) E. R. Lankester. "On the developmental History of the Mollusca." Phil. Trans., 1875.
Lamellibranchiata.
The ova of the Lamellibranchiata present several points of interest. They are developed in pouches of the ovary which are lined by a flattened germinal epithelium, or sometimes (?) a syncytium. Some of the cells of this epithelium enlarge and become ova, but remain attached to the walls of their pouches by protoplasmic stalks. Round the ovum there appears in some forms (Anodon, Unio) a delicate vitelline membrane, which is incomplete at the protoplasmic stalk, and is therefore perforated by an aperture which forms the micropyle. (Fig. 12.) As the ovum becomes ripe a large space filled with albuminous fluid becomes established between the ovum and its membrane, but the ovum remains attached to the membrane at the micropyle. In Scrobicularia (von Jhering, No. 25) the membrane round the ovum appears from the first as an albuminous layer, the outermost stratum of which becomes subsequently hardened as the vitelline membrane. In this form also the protoplasmic stalk becomes, in pouches largely filled with ova, extremely long. The ova become eventually detached by the stalk rupturing, and the portion of it which remains attached to the vitelline membrane falling off. The function of the stalk and of the micropyle during the development of the ovum is undoubtedly a nutritive one.
In Anodon and Unio yolk granules similar to those deposited in the protoplasm of the ovum are also found in the epithelial cells of the ovarian pouches (Flemming, 22), and there can be but little doubt that they are directly transported from these cells into the ovum. These cells would seem therefore to play much the same part as the yolk-glands of some Turbellarians (Prostomum caledonicum). In Scrobicularia yolk granules are not found in the epithelium of the pouches, but are contained in the dilated disc by which the ovum is attached to the wall of its pouch, as well as in the ovum itself.
[FIG. 12. MEDIUM-SIZED OVUM OF ANODONTA COMPLANATA. (After Flemming.)
mp. micropyle. gs. germinal spot.]
On the ovum becoming detached the micropyle still remains as an aperture, which probably has the function of admitting the spermatozoa.
The shape and form of the micropyle vary greatly. In Anodon and Unio it is a projecting trumpet-shaped structure, which after fertilization becomes shortened and reduced to a mere aperture which is finally stopped up. (Fig. 12.)
In other forms it is simply a perforation in the vitelline membrane which is sometimes very large. In a species of Arca, which I had an opportunity of observing at Valparaizo, it was equal to nearly the circumference of the ovum.
The eggs of the Lamellibranchiata are not only remarkable in the possession of a micropyle, but in certain peculiarities of the yolk and of the germinal vesicle.
In the fresh-water mussels there is usually found in young and medium-sized ova a peculiar lens-shaped body--Keber's corpuscle--which is placed immediately internal to the micropyle. It is probably in some way connected with the nutrition of the ovum, though the fact that it is not always present shews that it cannot be of great importance.
A dark body found by von Jhering in the neighbourhood of the germinal vesicle in the ripe ovum of Scrobicularia is probably of a similar nature to Keber's corpuscle. Both bodies may be placed in the same category as the so-called yolk nucleus of the spider's and frog's ova.
In all except the youngest ova of Anodon and Unio the germinal spot is composed of two nearly complete spheres united together for a small part of their circumference. (Fig. 12, gs.) The smaller of these has a higher refractive index than the larger, and often contains a vacuole: the two parts together appear to be the separated components (though not by simple division) of the primitive nucleolus. A nucleolus of this character is not universal amongst Lamellibranchiata, but a similar separation of the constituents of the germinal spot has been found by Flemming in Tichogonia, in which however the more highly refracting body envelopes part of the less highly refracting body in a cap-like fashion.
Gasteropoda.
The ova of the Gasteropoda are developed, like those of the Lamellibranchiata, from the epithelial cells of the ovarian acini or pouches. In the hermaphrodite forms both ova and spermatozoa are produced in the same pouches (fig. 13), some of the epithelial cells becoming ova and others spermatozoa. The ova are usually formed in the wall of the pouch, and the spermatozoa internally (Pulmonata) (fig. 13 A), or a further differentiation of parts may take place (fig. 13 B). The ova of Gasteropods are exceptional in the fact that a vitelline membrane is rarely or never developed around them. The ovum in its passage to the exterior becomes enclosed in a secretion of the albuminous gland, which hardens externally to form a special membrane.
[FIG. 13. FOLLICLES OF THE HERMAPHRODITE GLANDS OF GASTEROPODA. (From Gegenbaur.)
A. Of Helix hortensis. The ova (aa) are developed on the wall of the follicle, and the seminal masses (b) internally.
B. Of Aeolidia. The seminal portion of a follicle is beset peripherally by ovarian saccules (a). c. Common afferent duct.]
Cephalopoda.
Lankester (No. 32) has brought out some very interesting points with reference to the nutrition of the eggs of Sepia during their growth. The eggs develop in connective-tissue pouches which early give rise to a double pedunculated capsule of connective tissue. The cells of the inner layer of this capsule soon assume an epithelial character, and become a definite follicular epithelium, while between the two layers there penetrates a network of vascular channels. The follicular epithelium becomes after the establishment of these vascular channels folded in a most remarkable manner. The folds, which are shewn in section in fig. 14, ic, project into and nearly completely fill up the body of the ovum. An enormous increase is thus effected in the nutritive surface exposed by the epithelium. Each fold is thoroughly supplied with blood-vessels. The plications of the follicular epithelium give rise to a basket-work tracery on the surface of the ovum. During the stage when the follicular epithelium has the above structure, its cells have a character similar to that of the goblet-cells of a mucous membrane, and pour out their metamorphosed protoplasm into the body of the ovum.
[FIG. 14. TRANSVERSE SECTION THROUGH AN OVARIAN EGG OF SEPIA. (Copied from Lankester.)
o.c. outer capsular membrane. i.c. inner capsular membrane with follicular epithelium. b.v. blood-vessels in section between the outer and inner capsular membranes. c. vitellus.
The section shews the folds of the inner capsule with their epithelium, which penetrate into the substance of the ovum for the purpose of supplying it with nourishment.]
After the above mode of nutrition has gone on for a certain time a change takes place, and the ridges gradually disappear. This is caused by the epithelial cells passing off from the ridges into the protoplasm of the ovum; and becoming assimilated, after retaining their individuality for a longer or shorter period. When the absorption of the ridges is completed the surface of the ovum assumes a perfectly regular outline. The capsule of the ovum then bursts at the opposite pole to the peduncle, and the ovum falls into the oviduct.
The ova of the Cephalopoda, like those of the Gasteropoda, are quite naked, being without a vitelline membrane or chorion. The egg-capsule which is formed for them in their passage down the oviduct is perforated in Sepia by a micropylar aperture.
CHÆTOPODA.
(33) Ed. Claparède. "Les Annelides Chætopodes d. Golfe de Naples." Mém. d. l. Sociét. phys. et d'hist. nat. de Genève 1868-9 and 1870.
(34) E. Ehlers. Die Borstenwürmer nach system. und anat. Untersuchungen. Leipzig, 1864-68.
(35) E. Selenka. "Das Gefäss-System d. Aphrodite aculeata." Niederländisches Archiv f. Zool., Vol. II. 1873.
The ova of the Chætopoda are in most cases developed from the special tracts of the epithelial cells lining parts of the body cavity, which constitute a germinal epithelium (fig. 15). Very frequently (Aphrodite, Arenicola), as is so common in other types, these tracts of germinal cells surround the blood-vessels. In some cases the germinal epithelium thickens to form a compact organ, for which the outermost cells may form a more or less definite membranous covering (Oligochæta, etc.). The ova are formed by the enlargement, accompanied by other changes, of these germinal cells. During their early development the ova are frequently surrounded by a special capsule, which is often stalked, and provided at its attachment with a large micropylar aperture. In Aphrodite and Polynoe this arrangement, which is clearly connected with the nutrition of the ovum, is very easily seen. The ovum is dehisced into the body cavity by the bursting of its capsule or the rupture of the stalk. The capsule is always eventually thrown off; but a vitelline membrane is frequently developed after the detachment of the ovum into the body cavity. The vitelline membrane of Spio and other Polychæta is provided with an equatorial ring of ampulliform vesicles.
[FIG. 15. A PARAPODIUM OF TOMOPTERIS. (From Gegenbaur.)
o. Collection of germinal epithelial cells lining the body cavity.]
DISCOPHORA.
(36) H. Dorner. "Ueber d. Gattung Branchiobdella." Zeit. f. wiss. Zool., Vol. XV. 1865.
(37) R. Leuckart. Die menschlichen Parasiten.
(38) Fr. Leydig. "Zur Anatomie v. Piscicola geometrica, etc." Zeit. f. wiss. Zool., Vol. I. 1849.
(39) C. O. Whitman. "Embryology of Clepsine." Quart. J. of Micr. Sci., Vol. XVIII. 1878.
The ovary of the Discophora is formed of a mass of cells enveloped in a membranous sack. In Branchiobdella there is placed in the central axis of these cells a column of nucleated protoplasm from which the cells themselves are budded off. The development of the ovum takes place by the enlargement, etc. of one of the peripheral cells, which eventually bursts the wall of the sack and is freely dehisced into the body cavity.
In most other Leeches (except Piscicola and its allies) there is found a more specialized arrangement of the same nature as in Branchiobdella. There are one or more coiled egg-strings which lie freely in a delicate sack continuous with the oviduct. Each egg-string is formed of a central rachis and of a peripheral layer of cells[22]. The ova are formed by the enlargement of the peripheral cells accompanied by a deposition of food-yolk. Food-yolk appears to be formed in the rachis even more energetically than in the protoplasm of the ova. When ripe the ova fall into the ovarian sack.
[22] The rachis is stated by Whitman (No. 39), and other observers to be formed of nucleated protoplasm, but further investigations on this point are still required.
In Piscicola the development of the ovum is somewhat peculiar but resembles in certain respects that of Bonellia (p. 45). The ova are developed from the primitive germinal cells which fill up the ovarian sack. The nuclei in these cells increase in number, and a nucleated peripheral layer of each cell becomes separated from the central part, which also contains nuclei. This latter part next divides into numerous cells, of which one eventually forms the ovum, and the remainder constitute a mass of cells adjoining it as in Bonellia (fig. 16). This mass of cells eventually disappears, and is probably employed in the nutrition of the ovum.
The ovaries of the Leech appear to belong to the tubular type in that the ova are not formed from part of the epithelium lining the body cavity; but if, as seems probable, the true affinities of the Leeches are with the Chætopoda, the investment of the ovaries must be of a secondary nature. It should be noted that the ova are not, as in the ordinary tubular ovary, developed from the epithelium lining the ovarian tube.
GEPHYREA.
(40) Keferstein u. Ehlers. Zoologische Beiträge. Leipzig, 1861.
(41) C. Semper. Holothurien, 1868, p. 145.
(42) J. W. Spengel. "Beiträge z. Kenntniss d. Gephyreen." Beiträge a. d. zool. Station z. Neapel, Vol. I. 1879.
(43) J. W. Spengel. "Anatomische Mittheilungen üb. Gephyreen." Tagebl. d. Naturf. Vers. München, 1877.
In the Gephyrea, as in the Chætopoda, the ova are developed from the lining cells of the peritoneum and frequently from the cells surrounding parts of the vascular system (Bonellia, Thalassema). In many cases (Sipunculus, Phascolosoma, Echiurus) the main growth of the ovum takes place after it has been dehisced into the body cavity.
In Sipunculus the ova in the body cavity are surrounded by a follicle which is thrown off before they become ripe.
Brandt denies the existence of this follicle or rather its cellular nature. Spengel's (43) observations are conclusive in favour of the correctness of the original interpretation Of Keferstein and Ehlers. The follicles would seem to be formed after the ova have become free. In Phascolosoma there is no follicle (Semper, Spengel).
In both Phascolosoma and Sipunculus a vitelline membrane with radial pores--zona radiata--is formed, and in Phascolosoma the external part of this is separated off as a structureless vitelline membrane. The formation of both these membranes from the protoplasm of the ovum is rendered certain in the latter case by the absence of a follicular epithelium.
Some interesting observations on the growth and origin of the ovum in Bonellia have been made by Spengel.
[FIG. 16. FOLLICLE OF BONELLIA AT A MEDIUM STAGE OF DEVELOPMENT. (After Spengel.)
ov. ovum. fe. flattened follicular epithelium.]
The ova originate from certain cells (germinal cells) in the peritoneal investment of the ventral vessel, overlying the nervous cord. These cells, which are well marked off from the surrounding flattened peritoneal elements, increase in number by division, and form small masses surrounded by a follicle of peritoneal cells, and attached by a stalk to the peritoneum. The central cell of each mass grows larger than the rest, which arrange themselves in a columnar fashion round it; it is not, however, destined to become the ovum. On the contrary certain of the other cells adjoining the stalk grow larger, and finally one of these becomes distinguished as the ovum by its greater size and the character of its nucleus. The remainder of the larger cells become of the same size as their neighbours. The ovum now becomes more or less separate from the mass of germinal cells, rapidly grows in size, and soon forms the most considerable constituent of the follicle (fig. 16, ov). The remaining germinal cells are quite passive, and though, with the exception of the central cell, they do not appear to atrophy, they soon constitute a relatively small prominence on the surface of the ovum. By the rupture of the stalk the whole follicle becomes eventually detached, and the further development of the ovum takes place in the body cavity. A vitelline membrane is formed, and eventually the ovum is taken into the oviduct (segmental organ). At this time or slightly before, the follicle cells together with the germinal mass, which throughout exhibits no signs of atrophy, become thrown off, and the ovum is left invested in its vitelline membrane.
NEMATODA.
(44) Ed. Claparède. De la formation et de la fécondation des oeufs chez les Vers Nématodes. Genève, 1859.
(45) R. Leuckart. Die menschlichen Parasiten.
(46) H. Munk. "Ueb. Ei- u. Samenbildung u. Befruchtung b. d. Nematoden." Zeit. f. wiss. Zool., Vol. IX. 1858.
(47) H. Nelson. "On the reproduction of Ascaris mystax, etc." Phil. Trans. 1852.
(48) A. Schneider. Monographie d. Nematoden. Berlin, 1866.
The female organs consist as a rule of two cæcal tubes which unite before opening to the exterior. Each of these is divided into a vagina, uterus, oviduct, and ovary. The ovary constitutes the blind end of the tube, and is formed of a common protoplasmic column, holding a number of nuclei in suspension. The protoplasm becomes cleft around the nuclei in the uppermost part of the tube; the circumscription of the ova proceeds, however, very gradually, and since it commences at the periphery of the column the ova remain attached by stalks to a central axis with one end free. In this way there is formed a rod-like structure known as the rachis, which consists of a central axis with a series of half circumscribed ova radiately arranged round it. In the lowest part of the ovary the ova become completely isolated and form separate cells.
The protoplasm of the ova, which is clear in the terminal division of the ovary, becomes in most forms filled lower down with yolk-spherules secreted in the body of the ova. These commence to appear at the uppermost extremity of the rachis.
In some instances, e.g. Cucullanus elegans, yolk-spherules are not formed. In the Oxyuridæ the ova are directly segmented off from the terminal syncytium of protoplasm without the intervention of a rachis; and are therefore formed in the same way as amongst Trematodes, etc.
The origin of the membrane around the ova of the Nematoda has been much disputed.
At the time when the ovum is detached from the rachis no membrane is present, but it nevertheless appears from Schneider's observations that the region at which it is detached is softer than other parts, so that a kind of micropyle is here formed which disappears after impregnation. A delicate vitelline membrane then appears, around which there is subsequently established an egg-shell, which is usually stated to be formed as a secretion of the walls of the uterus; but Schneider and Leuckart have given strong grounds for believing that it is really a further differentiation of the vitelline membrane due to the activity of the protoplasm of the ovum. The originally single membrane becomes as it thickens split into two layers. The outer of these forms the true egg-shell, and the fertilization of the ovum appears to be a necessary prelude to its production. Round the egg-shell the walls of the uterus often secrete a special albuminous covering.
The egg-shell exhibits in many cases peculiar sculpturings as well as terminal prolongations.
INSECTA.
(49) A. Brandt. Ueber das Ei u. seine Bildungsstätte. Leipzig, 1878.
(50) T. H. Huxley. "On the agamic reproduction and morphology of Aphis." Linnean Trans., Vol. XXII. 1858. Vide also Manual of Invertebrated Animals, 1877.
(51) R. Leuckart. "Ueber die Micropyle u. den feinern Bau d. Schalenhaut bei den Insecteneiern." Müller's Archiv, 1855.
(52) Fr. Leydig. Der Eierstock u. die Samentasche d. Insecten. Dresden, 1866.
(53) Lubbock. "The ova and pseudova of Insects." Phil. Trans. 1859.
(54) Stein. Die weiblichen Geschlechtsorgane d. Käfer. Berlin, 1847.
[Conf. also Claus, Landois, Weismann, Ludwig (No. 4).]
The ovum of Insects has formed the subject of numerous investigations, and has played an important part in the controversies on the nature of the ovum.
The ovaries are paired organs, rarely directly connected, each consisting of more or fewer ovarian tubes which open into a common oviduct. The oviducts unite into a vagina, usually provided with a spermatheca and accessory glands, which need not be further alluded to. Each ovary is invested by a peritoneal covering, which assumes various characters, and either forms a loose network covering the whole or a special tunic round each egg-tube. It is continuous with the general peritoneal investment. Each ovarian tube (fig. 17) consists of three sections: (1) a terminal thread, (2) the terminal chamber or germogen, (3) the egg-tube proper.
[FIG. 17. A. OVARIAN TUBE OF THE FLEA, PULEX IRRITANS. (From Gegenbaur, after Lubbock.)
o. ovum. g. germinal vesicle.
B. OVARIAN TUBE OF A BEETLE, CARABUS VIOLACEUS. (After Lubbock.)
o. ovarian segment, formed of an ovum a, and a mass of yolk cells, b.]
The whole egg-tube is invested in a structureless tunica propria.
The terminal threads are fine prolongations of the ends of the egg-tubes usually continued close up to the heart. At their extremities they frequently anastomose, or even unite into a common thread. In some cases they are absent. They form either direct continuations of the germogen and have the same histological structure, or in other cases are simply prolongations of the tunica propria, and serve as ligaments.
The germogen usually consists of two parts: an upper, filled with nuclei imbedded in protoplasm, and a lower, in which distinct cells have become differentiated.
The lower part of the egg-tubes is filled with ova which advance in development towards the oviduct, and lie in chambers more or less distinctly constricted from each other. In these chambers there are in most forms in addition to the true ova a certain number of nutritive cells. The true egg-tubes are moreover lined by an epithelial layer which passes in and forms more or less complete septa between the successive chambers. The points which have been especially controverted are (1) the relation of the ovum to the germogen, and (2) the relation of the nutritive or yolk cells to the ovum. To the controversies on these points it will only be possible to give a passing allusion.
As has been already hinted there are two distinct types of ovaries, viz. those without the so-called nutritive or yolk cells and those with them[23].
[23] For a list of the genera with and without nutritive cells, vide Brandt, pp. 47 and 48.
The formation of the ovum is most simple in the type without yolk cells, which will for that reason be first considered (fig. 17 A).
The germogen is constituted of a number of nuclei imbedded in a scanty cementing protoplasm. In the lower part of the germogen the nuclei are larger, and become separated off from the nucleated protoplasm above, as distinct cells with a thin layer of protoplasm round the germinal vesicle. These cells are the ova. As they pass down the egg-tube their protoplasm increases in bulk, and they become isolated by ingrowths of the epithelial cells the origin of which is still uncertain, which form round each ovum a special follicle, so that the egg-tube is filled by a single row of ova each in an epithelial follicle (fig. 17 A). The larger the ova the more columnar is the epithelium of the follicle. As the oviductal extremity of the egg-tube is approached the ova increase in size, and their protoplasm is more and more filled with yolk particles.
In the lower part of the egg-tube the epithelium gives rise to a chorion.
The epithelium around each ovum has been spoken of as forming a follicle, and it is implied that the epithelium round each ovum travels down the egg-tube with the ovum. It is however by no means clear from the observations of the majority of writers that this is the case, and in fact the epithelium is generally spoken of as if it were simply the epithelium of the egg-tube. In favour of the view here adopted the following considerations may be urged.
Firstly, there is considerable evidence that the superficial layer of the germogen gives rise to the epithelial cells, simultaneously with the formation of the ova from the deeper layers.
Secondly, the fact that the epithelium grows in between the separate ova appears to render it almost certain that this part of the epithelium must travel down the egg-tubes with the ova.
Thirdly, the epithelium no doubt gives rise to the chorion, and considering the peculiar structure of the chorion, this seems possible only on the view that the epithelium travels down the egg-tube with the ova.
Fourthly, when, or even before, the egg is laid the epithelium undergoes atrophy, and the remains of it have been compared to the corpora lutea.
If the view about the epithelium here adopted is correct, the epithelium without doubt corresponds to the follicular epithelium of other ova, and has the same origin as the ova themselves.
The ovaries with yolk cells differ in appearance from those without, mainly in each ovarian chamber of an egg-tube containing two elements, usually more or less distinctly separated. These two elements are (1) at the lower end of the chamber, the ovum, and (2) at the upper, large cells which gradually disappear as the ovum grows larger (fig. 17 B).
The uppermost part of the egg-tube is formed, as in the previous type, by a mass of nucleated protoplasm, but the germinal cells formed from it do not all become ova. The germinal cells leave the germogen in batches, and in each batch one of the cells may usually be distinguished from the very first as the ovum; the remainder forming the nutritive cells. In the uppermost part of the egg-tube the whole mass of each batch is very small, and the successive batches are very imperfectly constricted from each other. Gradually however both the nutritive cells and the ovum grow in size, and then as a rule, the Diptera forming a marked exception, the chamber containing a batch becomes constricted into an upper section with the nutritive cells and a lower one with the ovum. The ovum in passing down the tube becomes gradually invested by a layer of epithelial cells, which in many cases pass in and partially separate the ovum from the nutritive cells. The epithelium appears not unfrequently to be continued as a flat layer between the nutritive cells and the wall of the egg-tube.
As was first shewn by Huxley and Lubbock, the protoplasm of the ovum is often continued up as a solid cord, which terminates freely between the nutritive cells, and serves to bring to the ovum the material elaborated by them. It is present in its most primitive form in the somewhat aberrant ovary of Coccus. In this ovary the terminal chamber is filled with cells which are united to a central rachis, as in Nematodes, and the prolongation from the ovum is continuous with this rachis. This cord is known as the yolk-duct (Dottergang) by German writers. Although it is not generally present in a distinct form, there is always a passage connecting the ovum and yolk cells, even when the follicular epithelium grows in and nearly separates them.
The number of nutritive cells varies from two (one ?) to several dozen. After they have reached a maximum they gradually atrophy, and are finally absorbed without apparently fusing directly with the ovum. The two types of insect ovaries appear fundamentally to differ in this. In the one type all the germinal cells develop into ova; in the other the quantity is, so to speak, sacrificed to the quality, and the majority of germinal cells are modified so as to subserve the nutrition of the few. It is still undecided whether the yolk cells absolutely elaborate yolk particles, or are merely conveyers of nutriment to the ovum.
The egg membranes of Insects present many points of interest, which are however for the most part beyond the scope of this work. There is always a chorion formed as a cuticular deposit of the follicle cells, which is frequently sculptured, finely perforated, etc., and is in many instances provided with a micropyle, developed, according to Leydig, at the upper end of the ovum.
Its development at this point appears to be due to the fact that the follicle is here incomplete; so that the cuticular membrane deposited by it is also incomplete.
A true vitelline membrane can in many instances be demonstrated (Donacia, etc.).
ARANEINA.
(55) Victor Carus. "Ueb. d. Entwick. d. Spinneneies." Zeit. f. wiss. Zool., Vol. II. 1850.
(56) v. Wittich. "Die Entstehung d. Arachnideneies im Eierstock, etc." Müller's Archiv. 1849.
[Conf. Leydig, Balbiani, Ludwig (No. 4), etc.]
The ova of many Araneina are remarkable for the presence in the ovum of the so-called yolk-nucleus. The ova develop from the epithelial cells lining the ovarian sack. Certain of these cells grow large and project outwards, invested by the structureless membrane of the ovarian wall. The stalks of projections so formed are turned towards the lumen of the ovary, and are plugged with the epithelial cells which line the ovarian sack. When ripe, the ova pass from their sacks into the cavity of the ovary. The yolk-nucleus, which appears very early, is a solid body present in the protoplasm of the ovum. It is not found in all genera of Araneina. At its full development it exhibits in the fresh condition a granular structure, but very soon shews an irregularly concentric stratification which becomes more marked on the addition of reagents. According to Balbiani this stratification is confined to the superficial layers, while internally there is a body with all the characters of a cell. The yolk-nucleus is still found in the nearly ripe ovum, though it always disappears before development commences. It is probably connected with the nutrition of the ovum, though nothing is certainly known about its function.
CRUSTACEA.
(57) Aug. Weismann. "Ueb. d. Bildung von Wintereiern bei Leptodora hyalina." Zeit. f. wiss. Zool., Vol. XXVII. 1876.
[For general literature vide Ludwig No. 4 and Ed. van Beneden, No. 1.]
Amongst the many interesting observations on the Crustacean ova I will only allude to those of Weismann on the ova of Leptodora, a well-known Cladoceran form.
The phenomena of the development of the ova in this form present a close analogy with those in Insects.
The ovary is formed of (1) a germogen containing at its upper end nucleated protoplasm and lower down germinal cells in groups of four; (2) of a portion formed of successive chambers in each of which there is a row of four germinal cells. Of the four cells only the third develops into an ovum; the remainder are used as pabulum. This is the mode of development in the summer. In the winter the sacrifice of a larger number of germinal cells is required for the development of the ova; and an ovum is produced only in the alternate chambers. In the chambers where an ovum will not be formed an epithelial investment becomes first established round the four germinal cells. The four cells then coalesce, and form a spherical ball of protoplasm from which portions are budded off and absorbed by the investing epithelial cells, which at the same time lose their nuclei. When the whole of the central ball is thus absorbed by the epithelial cells, the latter become used by the winter ovum as food. The winter ovum at its full development is formed of a central mass of food-yolk and superficial layer of protoplasm.
CHORDATA.
Urochorda. (Tunicata.)
(58) A. Kowalevsky. "Weitere Studien ü. d. Entwicklung d. Ascidien." Archiv f. mikr. Anat., Vol. VII. 1871.
(59) A. Kowalevsky. "Ueber Entwicklungsgeschichte d. Pyrosoma." Arch. f. mikr. Anat., Vol. XI. 1875.
(60) Kupffer. "Stammverwandtschaft zwischen Ascidien u. Wirbelthieren." Arch. f. mikr. Anat., Vol. VI. 1870.
(61) Giard. "Études critiques des travaux, etc." Archives Zool. expériment., Vol. I. 1872.
(62) C. Semper. "Ueber die Entstehung, etc." Arbeiten a. d. zool.-zoot. Institut Würzburg, Bd. II. 1875.
Cephalochorda.
(63) P. Langerhans. "Z. Anatomie d. Amphioxus lanceolatus," pp. 330-3. Archiv f. mikr. Anat., Vol. XII. 1876.
Craniata.
(64) F. M. Balfour. "On the structure and development of the Vertebrate Ovary." Quart. J. of Micr. Science, Vol. XVIII. 1878.
(65) Th. Eimer. "Untersuchungen ü. d. Eier d. Reptilien." Archiv f. mikr. Anat., Vol. VIII. 1872.
(66) Pflüger. Die Eierstöcke d. Säugethiere u. d. Menschen. Leipzig, 1863.
(67) J. Foulis. "On the development of the ova and structure of the ovary in Man and other Mammalia." Quart. J. of Micr. Science, Vol. XVI. 1876.
(68) J. Foulis. "The development of the ova, etc." Journal of Anat. and Phys., Vol. XIII. 1878-9.
(69) C. Gegenbaur. "Ueb. d. Bau u. d. Entwicklung d. Wirbelthiereier mit partieller Dottertheilung." Müller's Archiv, 1861.
(70) Alex. Götte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.
(71) W. His. Untersuchungen üb. d. Ei u. d. Eientwicklung bei Knochenfischen. Leipzig, 1873.
(72) A. Kölliker. Entwicklungsgeschichte d. Menschen u. höherer Thiere. Leipzig, 1878.
(73) J. Müller. "Ueber d. zahlreichen Porenkanäle in d. Eikapsel d. Fische." Müller's Archiv, 1854.
(74) W. H. Ransom. "On the impregnation of the ovum in the Stickleback." Pro. R. Society, Vol. VII. 1854.
(75) C. Semper. "Das Urogenitalsystem d. Plagiostomen, etc." Arbeiten a. d. zool.-zoot. Instit. Würzburg, Vol. II. 1875.
[Cf. Ludwig, No. 4, Ed. van Beneden, No. 1, Waldeyer, No. 6, &c.]
There are some very obscure points connected with the growth of the ovum of the Tunicata. When quite young the ovum is a naked cell with a central nucleus containing a single large nucleolus. Around it is a flat follicular epithelium enclosed in a membrana propria folliculi. The follicle cells soon become larger and give rise to an envelope round the egg of the nature of a chorion. At the same time they frequently become cubical or even columnar, and filled with numerous vacuoles.
During or after the completion of the above changes a number of bodies usually spoken of as test-cells make their appearance in the superficial protoplasm of the egg, which by the time the egg is ripe arrange themselves in many species as a definite layer round the periphery of the ovum. These bodies have received their name from the opinion, now known to be erroneous (Hertwig and Semper), that they eventually migrated into the test or mantle of the embryo which becomes developed round the ovum. By Kowalevsky (No. 58) these bodies are regarded as true cells, and are believed to be formed by some of the cells of the original follicular epithelium making their way into the vitellus of the ovum and multiplying there. By Kupffer (No. 60), and Giard (No. 61), and Fol, they are also regarded as true cells but are believed to originate spontaneously in the vitellus. Finally by Semper they are believed not to be cells, but to be amoeboid protoplasmic bodies which are pressed out from the vitellus under the stimulus of the sea-water or otherwise.
They do not according to this author naturally appear till the ovum is quite ripe, though they can be artificially produced at an earlier period by the action of reagents or sea-water. When produced in the natural course of things the vitellus undergoes a contraction. They are without any apparent function, and play no part in the embryonic development. Semper's results are very peculiar, but owing to the careful study which his paper displays they no doubt deserve attention. Further investigations are however very desirable. Kowalevsky from his researches on Pyrosoma (No. 59) adheres to his first opinion, though he abandons the view that these cells are connected with the formation of the test.
In the passage of the egg through the oviduct the vacuolated follicle cells grow out into very peculiar long processes or villi. In Ascidia canina these processes become as long as the whole diameter of the vitellus (Kupffer, No. 60).
In Amphioxus and the Craniata the ova are developed as in the Chætopoda, Gephyrea, etc., from specialized germinal cells of the peritoneal epithelium.
In Amphioxus the germinal epithelium which constitutes the essential part of the ovary is divided into a number of distinct segments: in the Craniata no such division is observable.
In young examples of Amphioxus the generative organs are in an indifferent condition, and the two sexes cannot be distinguished. They form isolated horse-shoe shaped masses of cells, which occupy a position at the base of the myotomes, in the intervals between the successive segments; and extend from the hinder end of the respiratory sack to the abdominal pore. They are situated in the proper body cavity, and are surrounded by the peritoneal membrane. Each generative mass is at first solid, and is formed of an outer layer of more flattened cells and an inner mass of large rounded or polygonal cells. In its interior there appears at a somewhat later period a central cavity. After the cavity has appeared the sexes can be distinguished by the different behaviour of the cells.
In all the Craniata, the ovary forms a paired ridge (unless single by abortion or fusion) attached by a mesentery to the dorsal wall of a more or less extended region of the abdominal cavity. This ridge is at first identical in the two sexes, and arises at an early period of embryonic life. It is essentially formed of a thickening of the peritoneal epithelium, and in Osseous Fish, Ganoids (?) and Amphibia the ovary remains during embryonic life nearly in this condition, though a small prominence of the adjacent stroma also becomes formed. In other Craniata the ridge, though at first in this condition, very soon becomes much more prominent, and is formed of a central core of stroma enclosed in the germinal epithelium (fig. 18).
[FIG. 18. TRANSVERSE SECTION THROUGH THE OVARY OF A YOUNG EMBRYO OF SCYLLIUM CANICULA, TO SHEW THE PRIMITIVE GERMINAL CELLS (po) LYING IN THE GERMINAL EPITHELIUM ON THE OUTER SIDE OF THE OVARIAN RIDGE.]
The thickened germinal epithelium gives rise (in the case of the female) to the ova and the follicular epithelium. Whether the genital ridge is provided with a core of stroma or no, the germinal epithelium is always in contact on one side with the stroma, from which it is at first separated by a well-marked boundary line; but after a certain time there appear numerous vascular ingrowths from the stroma, which penetrate through all parts of the germinal epithelium, and break it up into a sponge-like structure formed of trabeculæ of germinal epithelium interpenetrated by vascular strands of stroma. The trabeculæ of the germinal epithelium form the egg-tubes of Pflüger.
With reference to the distribution of the stroma in the germinal epithelium, it may be said in a general way that there is a special layer close to the surface of the ovary, which, after the formation of fresh ova has nearly ceased, completely isolates a superficial layer of the germinal epithelium from the deeper and major part of it. The superficial layer is frequently (but erroneously) regarded as constituting the whole of the germinal epithelium. The layer of stroma below the superficial epithelium forms in the mammalian ovary the tunica albuginea. As the follicles are formed. in the trabeculæ of germinal epithelium the stroma grows in around them, and forms for each one of them a special tunic.
The adult ovaries differ in a corresponding manner to the embryonic genital ridges as to the presence of a core of stroma. The ovaries which are without such a core in the embryo, are also without it in the adult, and are formed of a double layer of tissue entirely derived from the germinal epithelium with its ingrowths of stroma, and composed, for the most part, of ova in all stages of development. In the case of the other ovaries there is a hilus of stroma--the zona vasculosa--internal to the egg-bearing region.
In Mammalia, proportionately to the ovary, the zona vasculosa is at a maximum, and in Birds and Reptiles it is relatively far less developed. In these forms the germinal epithelium covers the whole surface of the ovary. In Elasmobranchii the structure of the ovary is somewhat different, owing to the presence in the ovarian ridge of a large quantity of a peculiar lymphatic tissue, which has no homologue in the other ovaries; and still more to the fact that the true germinal epithelium is in most forms entirely confined to the outer surface of the ovary, on which it forms a layer of thickened epithelium in the embryo (fig. 17), and of ovigerous tissue in the adult.
In the ovary of Mammalia and Reptilia and possibly other forms there are present in the zona vasculosa during embryonic life cords of epithelial tissue derived from the Malpighian bodies; these cords have no function in the female, but in the male assist in forming the seminiferous tubules.
In considering the development of the ova it is again convenient to distinguish between Amphioxus and the Craniata.
In Amphioxus the germinal cells destined to become ova are first distinguished by the larger size of their germinal vesicles and by the presence of certain refracting granules in their protoplasm. They subsequently rapidly enlarge and form protuberances on the surface of the ovary, which are enveloped for three-quarters of their circumference by the flattened epithelioid cells of the peritoneal membrane, which thus form a kind of follicle. As the ova become ripe yolk granules are deposited in their protoplasm, first in the superficial layer and subsequently throughout. The germinal vesicle also passes from the centre to the surface. A vitelline membrane is formed when the ova are mature.
In the Craniata the ova are developed from the cells of the germinal epithelium. In the types with larger ova (Teleostei, Elasmobranchii, Amphibia, Reptilia, Aves), at a very early period, sometimes (Elasmobranchii) even before the formation of the genital ridge, certain of the cells which are destined to form ova become distinguished by their greater size, and by the possession of an abundant clear protoplasm and a large spherical granular nucleus. (Fig. 18, po.) Such special cells form primitive germinal cells, and are common to both sexes.
For a considerable period after their first formation these cells remain stationary in their development; but their number increases, partly, it appears, by an addition of fresh ones, and partly by division. Owing to the latter process the germinal cells come to form small masses or nests. The following description of the further changes of these cells in the female refers in the first instance to Elasmobranchii, but holds good in most respects for other types as well.
It is convenient to distinguish two modes in which the primitive germinal cells may become converted into permanent ova, though the morphological difference between the two modes is of no great importance.
[FIG. 19. SECTION THROUGH PART OF THE GERMINAL EPITHELIUM OF THE OVARY OF SCYLLIUM AT THE TIME WHEN THE PRIMITIVE GERMINAL CELLS ARE BECOMING CONVERTED INTO OVA.
nn. Nests formed of agglomerated germinal cells. The nuclei of these cells are imbedded in undivided protoplasm. do. developing ova. o. ovum with follicle. po. primitive germinal cell. dv. blood-vessels.]
In the first mode the protoplasm of all the cells forming a nest unites into a single mass containing the nuclei of the previously independent ova (fig. 19, nn). The nuclei in the nest increase in number, probably by division, and at the same time the nest itself increases in size. The nuclei while increasing in number also undergo important changes. A segregation of their contents takes place, and the granular part (nuclear substance) forms a mass close to one side of the membrane of the nucleus, while the remainder of the nucleus is filled with a clear fluid. The whole nucleus at the same time increases somewhat in size. The granular mass gradually assumes a stellate form, and finally becomes a beautiful reticulum, of the character so well known in nuclei (fig. 19, do). Two or three special nucleoli are present, and form the nodal points of the reticulum, while its meshes are filled up with the clear fluid constituents of the nucleus. Not all the nuclei undergo the above changes; but some of them stop short in their development, undergo atrophy, and appear finally to be absorbed as pabulum by the protoplasm of the nest. Such nuclei in a state of degeneration are shewn in fig. 19. Thus only a few nuclei out of a nest undergo a complete development. At first the protoplasm of the nest is clear and transparent, but as the nuclei undergo their changes the protoplasm becomes more granular, and a specially large quantity of granular protoplasm is generally present around the most developed nuclei, and these with their protoplasm gradually become constricted off from the nest, and constitute the permanent ova (fig. 19, do). The relative number of ova which may develop from a single nest is subject to great variation. The object of the whole occurrence of the fusion of primitive ova and the subsequent atrophy of some of them is to ensure the adequate nutrition of a certain number of them.
In the second and rarer mode of development of permanent ova from primitive germinal cells, the nuclei and protoplasm undergo the same changes as in the first mode, but the cells either remain isolated, and never form part of a nest, or form part of a nest in which no fusion of protoplasm takes place, and in which all the cells develop into permanent ova.
The isolated ova and nests are situated, during the whole of the above changes, amongst the general undifferentiated cells of the germinal epithelium, but as soon as a permanent ovum becomes formed the cells adjoining it arrange themselves around it as a special layer, and so give rise to the epithelium of the follicle (fig. 19, o). The growths of stroma into the germinal epithelium appear shortly after the formation of the earlier follicles.
Mammalia. The development of the ovary in Mammalia differs mainly from that just described in that the formation of primitive germinal cells from the indifferent cells of the germinal epithelium takes place at a relatively much later period.
The stroma grows into the germinal epithelium while it is still formed of rounded indifferent cells, and divides it into trabeculæ as described above. At a later period a number of the cells in the deeper layer of the epithelium, as well as certain cells in the superficial part, become primitive germinal cells, while the remainder of the cells become smaller and are destined to form the follicle cells.
The most conspicuous primitive germinal cells are situated in the superficial layer of epithelium; and the primitive germinal cells in the deeper layers of the germinal epithelium are not nearly so marked as in most Craniata, so that it is difficult in some cases to be sure of their destination till their nucleus commences to undergo its characteristic metamorphosis.
The change of the primitive ova into permanent ova takes place in the same manner in Mammals as in Elasmobranchii, except that the fusion of the primitive ova into polynuclear masses is much rarer. The formation of the at first quite simple follicles takes place while the ova are still aggregated in large masses; and the first follicles are formed in the innermost part of the germinal epithelium. Soon after their formation the follicles become isolated by connective-tissue growths.
Post-embryonic development of the ova.
The ova of the Vertebrata differ greatly in size and structure. The differences in size depend upon the quantity of the food-yolk. In the Amphioxus and Mammalia, in which the ova are smallest, the comparatively insignificant amount of food-yolk is distributed uniformly through the ovum. A larger quantity of it is present in the ova of Amphibia, Marsipobranchii and Teleostei, and it attains an immense development in the ova of Elasmobranchii, Reptilia, and Aves.
The food-yolk originates from a differentiation of the protoplasm of the egg. It arises as a number of small highly refracting particles in a stratum slightly below the surface.
In the Mammalian ovum these particles spread through the protoplasm of the egg, but do not attain any considerable development. In other forms the case is different. In Elasmobranch Fishes the refracting particles appear to develop into vesicles, in the interior of which there arise solid oval or even rectangular highly refracting bodies, in the substance of which a stratification may usually be observed, which gives them an appearance not unlike that of striated muscle. In Teleostei the yolk assumes very different characters in different cases. It is often formed of larger or smaller vesicles containing in their interior other bodies. Stratified plates like those of Elasmobranchii are also not uncommon. In the ripe ovum of Teleostei the food-yolk usually resolves itself into a large vitelline sphere, which occupies the greater part of the ovum, and is formed of a highly refracting fluid material which coagulates on the addition of water. It contains in many instances one or more highly refracting bodies known as oil globules, and is invested by a granular protoplasmic layer continuous with the germinal disc, in which a number of normal yolk-spherules are frequently present. In the ovum of the Herring[24] no distinct investing protoplasmic layer or germinal disc is present till after impregnation, but the ovum is formed of a superficial layer with minute yolk-spherules, and of a central portion with larger yolk-spheres.
[24] Kupffer, Laichen u. Entwicklung des Ostsee-Härings. Berlin, 1878.
In Amphibia the yolk very often appears in the form of oval or quadrilateral plates. In Reptilia the yolk-spherules are vesicles, somewhat similar to the white yolk-spheres of Aves, but as a rule without the highly refracting spheres in their interior. The peculiar and complicated arrangement and structure of the white and yellow yolk in Birds is fully described in the "Elements Of Embryology," and it need only be said that the yolk develops in Birds in the same manner as in other types, and that at first all the yolk-spherules appear in the form of white yolk. The yellow yolk-spheres are a peculiar modification of white yolk-spheres, formed comparatively late in the development of the egg (fig. 20).
[FIG. 20. YOLK ELEMENTS FROM THE EGG OF THE FOWL.
A. Yellow yolk. B. White yolk.]
In the eggs of many Amphibia a dark granular mass known as the yolk nucleus makes its appearance; and is supposed, without any very clear evidence, to be related to the formation of the yolk.
A body in the form of a shell enclosing a dark nucleus, which is perhaps of the same nature, has been described by Eimer in the Reptilian egg: it eventually resolves itself into a number Of angular fragments. In Elasmobranchii a similar body is perhaps present.
The food-yolk just described is imbedded in the active protoplasmic portion of the body of the ovum. In the case of the mammalian ovum the food-yolk is fairly uniformly distributed, but in the case of all other craniate ova the protoplasm of the ovum is especially concentrated at one pole, which is known as the upper or animal pole, and the food-yolk is more especially concentrated at the opposite pole. The Herring's ovum forms an apparent exception to this statement, in that the concentration of the protoplasm to form the germinal disc does not take place till after impregnation. In Amphibia the animal pole is mainly marked by the smaller size of the yolk-spherules, but in most other forms a small portion of the ovum in the region of the germinal vesicle is nearly free from yolk-spherules, and then forms a more or less specialized part known as the germinal disc. In Aves, Reptilia, and Elasmobranchii the germinal disc shades off insensibly into the yolk; but in Teleostei it is more sharply marked off, and is continued more or less completely round the periphery of the ovum. In ova with true germinal discs it is the germinal disc alone which undergoes segmentation. The protoplasm of vertebrate ova frequently exhibits a reticulate or sponge-like structure (fig. 21) and the reticulum in many cases, e.g. Elasmobranchii and Reptilia, serves to hold the yolk-spheres together. In the Tench it has been observed by Bambeke to penetrate into the vitelline sphere.
In the ova of the Craniata the germinal vesicle is generally polynucleolar. In Amphioxus and Petromyzon there is however but a single nucleolus, and in Mammalia there is usually one special nucleolus and two or three accessory ones. The opposite extreme is reached in many osseous fish where the nucleoli are extremely numerous. The protoplasmic reticulum of the embryonic germinal vesicle may in some instances be retained till the ovum is nearly ripe, but usually assumes a very granular form. It is at first connected with the nucleoli which form nodal points in it, but this relation cannot always be detected in the later stages. A membrane, which in the case of the larger ova becomes very thick, is always present round the germinal vesicle. It is said to be perforated in some Reptilian ova (Eimer). As to the position of the germinal vesicle, it is at first situated in the centre of the ovum, but always eventually travels to the animal pole, and as the egg becomes ripe undergoes changes which will be more especially detailed in the next chapter. In the ova with a large amount of food-yolk it assumes an eccentric position very early.
The homologies of the primary egg membranes of Craniata are still involved in some obscurity. There seem to be three membranes, which may all coexist, and of which one or more are almost always present. These membranes are--
(1) An outermost usually homogeneous non-perforated membrane, which is by most authors regarded as a chorion, but is probably a vitelline membrane--by which name I shall speak of it.
(2) A radiately striated membrane (internal to the former when the two coexist) which can be broken up into a series of separate columns. These give to the membrane its radiate striation, but it is probable that between the columns there are pores sufficiently large to admit of the passage of protoplasmic filaments. This membrane will be spoken of as the zona radiata. It is a differentiation of the outermost layer of the yolk.
(3) Within the zona radiata a third and delicate membrane is occasionally found, especially when the ovum is approaching maturity.
[FIG. 21. SECTION THROUGH A SMALL PART OF THE SURFACE OF AN OVUM OF AN IMMATURE FEMALE OF SCYLLIUM CANICULA.
fe. follicular epithelium. vt. vitelline membrane. Zn. zona radiata. yk. yolk with protoplasmic network.]
In Elasmobranchii the first membrane to be formed is the vitelline membrane, which appears in some instances before the formation of the follicle--a fact which appears to shew that it is really formed as a differentiation of the protoplasm of the egg. In most Elasmobranchii this membrane attains a very considerable development. A zona radiata is generally (if not always) present in Elasmobranchii, but arises at a later period than the vitelline membrane (fig. 21, Zn). The zona radiata always disappears long before the ovum is ripe. The vitelline membrane also gradually atrophies, though it lasts much longer than the zona radiata. When the egg is taken up by the oviduct all trace of both membranes has vanished. In Reptilia precisely the same arrangements of the membranes are found as in Elasmobranchii, except that as a rule the zona radiata is relatively more important. The vitelline membrane is thin except in the Crocodilia. The third innermost membrane is found according to Eimer in many Reptilia. In birds both vitelline membrane and zona radiata are present, but the latter atrophies early, leaving the former as the sole membrane when the egg is ripe.
In osseous fish the vitelline membrane is usually either absent or may perhaps in some instances, e.g. the Perch, be imperfectly represented. In the ripe ovum of the Herring there is a distinctly developed membrane external to the zona radiata which is probably the vitelline membrane. The zona radiata attains a very great development, and is generally provided with knobs of various shapes on its outer surface. A delicate membrane internal to this--my third membrane--has often been described, but there is still some doubt about its existence. In some cases an external less granular layer of the ovum itself has been described as a special membrane. In the Perch a peculiar mucous capsule, penetrated by irregular branched prolongations of the follicle cells, is present in addition to the ordinary membranes. In Petromyzon a zona radiata appears to be present, which in the adult is divided into two layers, both of them radiately striated according to Calberla, but according to Kupffer and Benecke the outer one is not perforated, and would appear therefore to be a vitelline membrane as defined above. A delicate membrane is formed at a comparatively late period around the ova of the Amphibia, and is stated (Waldeyer, No. 6, and Kolessnikow) to have a delicate radial striation. It probably corresponds with the zona radiata.
In Mammalia a radiately striated membrane--the zona radiata--is generally described as being present, and internal to it, in the nearly ripe egg, a delicate membrane has been shewn by E. van Beneden to exist. Externally to the zona radiata there may be observed a granular membrane irregular on its outer surface on which the cells of the discus are supported. This membrane is more or less distinctly separated from the zona radiata; and by tracing back its development it appears very probable that it is the remnant of the first-formed membrane in the very young ovum, and therefore the vitelline membrane.
A micropyle (first discovered by Ransom, No. 74) is present in a large number of osseous fish and in Petromyzon (Calberla). Doubts have been thrown on its existence in the latter form by Kupffer and Benecke; and at any rate it would only seem to perforate the zona radiata. In the osseous fish in which it has been detected, Salmonidæ, Percidæ (Gasterosteus), Clupeidæe, etc., it forms a minute perforation of the zona radiata at the animal pole, just large enough to admit a single spermatozoon. Its characters differ slightly in different cases, but there is usually a shallow depression, in the centre of which it is situated.
The eggs of all Craniata (except Petromyzon (?)) appear to be enclosed in a cellular envelope known as the follicle. The cells which form this are, as has been already explained, derived from the germinal epithelium[25], and frequently arrange themselves around the ovum before the appearance of the growths of stroma into the epithelium. All young follicles are nearly alike, but as they grow older they exhibit various modifications in the different groups. They retain their simplest condition as a flat epithelial layer in most osseous fish and Amphibia. In most other forms the cells become at some period columnar, and are generally arranged in two or more layers. There is formed externally to the epithelium a delicate membrane--the membrana propria folliculi--which is in its turn enclosed in a vascular connective-tissue sheath.
[25] For the different views maintained by Foulis, Kölliker, etc. the reader is referred to the writings of these authors. The grounds for the view here adopted will be found in my paper (No. 64).
In Elasmobranchii and many Reptilia (Lacertilia, Ophidia) some of the cells become much larger than the others, and assume a funnel-shaped form with the narrow end in contact with the egg membrane. These large cells, which have a regular arrangement in the epithelium, are probably in some way connected with the nutrition. They have only been noticed in large-yolked ova. Many observers have described prolongations of the follicle cells through the pores of the zona radiata in Aves, Reptilia and Teleostei.
The most remarkable modification of the follicle is that which is found in Mammalia. At first the follicle is similar to that of other Vertebrata, and is formed of flat cells derived from the germinal cells adjoining the ovum. These cells next become columnar and then one or two layers deep. Later they become thicker on one side than on the other, and there appears in the thickened mass a cavity, which gradually becomes more distended and is filled with an albuminous fluid. As the cavity enlarges, the ovum with several layers of cells around it forms a prominence projecting into it. The whole structure with its tunic is known as the Graafian follicle. The follicle cells are known as the membrana granulosa, and the projection, in which the ovum lies, as the discus or cumulus proligerus. The cells of the discus in immediate contiguity to the ovum usually form a more or less specialized layer and are somewhat more columnar than the adjoining cells.
THE SPERMATOZOON.
Although there is no doubt that the spermatozoon in most instances plays as important a part as the ovum in influencing the characters of the organism which is evolved from the coalesced product of the ovum and spermatozoon, yet the actual form of the spermatozoon has not, like the form of the ovum, a secondary influence on the early phases of development. A comparative history of the spermatozoon is therefore of less importance for my purpose than that of the ovum; and I shall confine myself to a few remarks on its general structure, and mode of growth. The primary origin of the male germinal cells, and their relation to the sperm-forming cells, is dealt with in the second part of the treatise.
Although the minute size of most spermatozoa places great difficulties in the way of a satisfactory investigation of them, yet there can be but little doubt that they always have the value of cells. In the vast majority of instances the spermatic cell or spermatozoon is composed of (1) a spherical or oval portion known as the head, formed of a nucleus enveloped in an extremely delicate layer of protoplasm, and (2) of a motile protoplasmic flagellum known as the tail; which together with the investing layer of the head forms the body of the cell.
As might be anticipated, the proportion, size, and relations of the parts of the spermatozoon are subject to great variations. The head is often extremely elongated; and it is in many cases rather on theoretical grounds, than as a result of actual observation, that a protoplasmic layer is stated to be continued round the nucleus which forms the main constituent of the head. In some of the elongated forms of spermatozoa, e.g. in Insecta, there is no marked distinction, except in the character of the protoplasm, between the head and the tail. A connecting element is frequently interposed between the head and tail, which appears however to be constituted of the same material as the tail, and sometimes forms a thickening on the tail close below the head (Amphioxus). A very remarkable modification of the tail is found in many Amphibia, Reptilia and Mammalia. In these types there is attached to what appears to be a normal tail a delicate membrane, the outer edge of which is thickened to form a kind of secondary filament. In the living spermatozoon this filament is in a state of constant movement. The membrane winds spirally round the tail.
In the majority of forms the tail of the living spermatozoon exhibits sinuous cilia-like movements. In two groups the movements are however of an amoeboid character. These groups are the Nematoda and the Crustacea; and the spermatozoa in both of them frequently present very abnormal forms. In Nematoda they are pear-shaped, cylindrical, spine-shaped, etc., and are mainly formed of protoplasm with a highly refracting nucleus. In the Crustacea the variations of form are still greater. In the Malacostraca they are sometimes simply spherical (Squilla), while in Astacus and a large number of Decapoda they are composed of a nucleated body with stellate rays. In Paludina amongst the Mollusca there are two forms of completely developed spermatozoa existing side by side in the same individual.
The spermatozoa are formed by the breaking up of the male germinal cells, or of cells secondarily derived from them by division. The cells which directly give rise by division to the spermatozoa may be called spermospores and are equivalent to the ova or oospores.
Amongst the Sponges (Halisarca, Schultze, No. 141) a germinal cell, similar to that which in the female becomes an ovum, repeatedly divides and eventually gives rise to a ball of cells (a spermosphere or sperm-morula), each constituent cell of which becomes converted into a spermatozoon, and may be designated by the special term 'spermoblast.'
In most Hydrozoa the subepithelial epiblastic cells become converted into germinal cells (spermospores), and then break up to form spermoblasts, each of which becomes a spermatozoon.
In most higher Metazoa the spermospores usually form the epithelium of an ampulla or tube, though more rarely (many Chætopoda, Gephyrea, etc.) they may be derived from cells lining the body cavity, as in the case of ova. The spermatozoa are formed either by the direct division of the spermospores into a number of cells, spermoblasts, each of which grows into a spermatozoon; or by the nucleus of the spermospore becoming subdivided within the cell body, the latter differentiating itself into the tails of the spermatozoa while the segments of the nucleus give rise to the main part of the heads.
In many instances interstitial cells which do not give rise to spermatozoa, are intermingled with the spermospores.
In a good many cases, as first pointed out by Blomfield[26], the whole of each spermospore does not become converted into spermatozoa, but part, either with or without a segment of the original nucleus, remains passive, and carrying as it does the off-budded spermoblasts may be called the 'sperm-blastophor.' This passive portion of protoplasm is not employed in the regeneration of the spermoblast. This very singular phenomenon has been observed in Elasmobranchii, the Frog, the Earthworm, Helix, etc.[27], and probably has a much wider extension. In Elasmobranchii (Semper) the passive portions of protoplasm are nucleated, and are placed on the outer side of the columnar spermospores which line the testicular ampullæ; they are not distinctly differentiated till the nuclei, segmented from the nucleus of the primitive spermospore to form the heads of the spermatozoa, have become fairly numerous. In the Frog the passive blastophor also occurs as a nucleated mass of protoplasm on the outer side of the spermospore. In the Earthworm the blastophor forms a central non-nucleated portion of the spermospore; and the whole periphery of each spermospore becomes converted into spermoblasts.
[26] Quart. Journ. of Micro. Science, Vol. XX. 1880.
[27] Blomfield, loc. cit., p. 83, states that he has observed this fact in Lumbricus, Tubifer, Hirudo, Helix, Arion, Paludina, Rana, Salamandra, and Mus.
It has been already stated in the introduction that the male and female generative products are homodynamous, but the consideration of the development of the products in the two sexes shews that a single spermatozoon is not equivalent to an ovum, but rather that the whole of the spermatozoa derived from a spermospore are together equivalent to one ovum.
II. THE MATURATION AND IMPREGNATION OF THE OVUM
Maturation of the ovum and formation of the polar bodies.
In the preceding chapter the changes in the ovum were described nearly up to the period when it became ripe, and ready to be impregnated. Preparatory to the act of impregnation there take place however a series of remarkable changes, which more especially concern the germinal vesicle.
The attention of a large number of investigators has recently been directed to these changes as well as to the phenomena of impregnation. The results of their investigations will be described in the present chapter; but for an historical account of these investigations, as well as for a determination of the delicate questions of priority, the reader is referred to Fol's memoir (No. 87), and to a paper by the author (No. 81).
[FIG. 22. RIPE OVUM OF ASTERIAS GLACIALIS ENVELOPED IN A MUCILAGINOUS ENVELOPE, AND CONTAINING AN ECCENTRIC GERMINAL VESICLE AND GERMINAL SPOT (copied from Fol).]
The nature of the changes which take place in the maturation of the ovum may perhaps be most conveniently displayed by following the history of a single ovum. For this purpose the eggs of Asterias glacialis, which have recently formed the subject of a series of beautiful researches by Fol (87), may be selected.
The ripe ovum (fig. 22), when detached from the ovary is formed of a granular vitellus enveloped in a mucilaginous coat, the zona radiata. It contains an eccentrically-situated germinal vesicle and a germinal spot. In the former is present the usual protoplasmic reticulum. As soon as the ovum reaches the sea-water the germinal vesicle commences to undergo a peculiar metamorphosis. It exhibits frequent changes of form, the reticulum vanishes, its membrane becomes gradually absorbed, its outline indented and indistinct, and finally its contents become to a certain extent confounded with the vitellus (fig. 23).
[FIG. 23. TWO SUCCESSIVE STAGES IN THE GRADUAL METAMORPHOSIS OF THE GERMINAL VESICLE AND SPOT OF THE OVUM OF ASTERIAS GLACIALIS IMMEDIATELY AFTER IT IS LAID (copied from Fol).]
The germinal spot at the same time loses its clearness of outline and gradually disappears from view.
At this stage, and between it and the stage represented in fig. 26, the action of reagents brings to light certain appearances the nature of which is not yet fully cleared up for Asterias, which have been described somewhat differently by Fol for Ast. glacialis and Hertwig for Asteracanthion.
Fol finds immediately after the stage just described that a star is visible between the remains of the germinal vesicle and the surface of the egg, which is connected with an imperfectly-formed nuclear spindle extending towards the germinal vesicle[28]. At the end of the nuclear spindle may be seen the broken up fragments of the germinal spot.
[28] By the term 'nuclear spindle' I refer to the peculiar form of a double striated cone assumed by the nucleus just before division, which is no doubt familiar to all my readers. I use the term star for the peculiar stellate figure usually visible at the poles of the nuclear spindle. For a further description of these parts the reader is referred to Chapter IV.
[FIG. 24. OVUM OF ASTERIAS GLACIALIS SHEWING THE CLEAR SPACES IN THE PLACE OF THE GERMINAL VESICLE. FRESH PREPARATION (copied from Fol).]
At a slightly later stage, in the place of the original germinal vesicle there may be observed in the fresh ovum two clear spaces (fig. 24), one ovoid and nearer the surface, and the second more irregular in form and situated rather deeper in the vitellus. In the upper space parallel striæ may be observed. By treatment with reagents the first clear space is found to be formed of a horizontally-placed spindle with two terminal stars, near which irregular remains of the germinal spot may be seen. Slightly later (fig. 25) there may be seen on the lower side of the spindle a somewhat irregular body, which may possibly be part of the remains of the germinal spot, though Fol holds that it is probably part of the membrane of the germinal vesicle. The lower clear space visible in the fresh ovum now contains a round body, fig. 25. Fol concludes that the spindle is formed out of part of the germinal vesicle and not from the germinal spot, while he sees in the round body present in the lower of the two clear spaces the metamorphosed germinal spot. He will not, however, assert that no fragment of the germinal spot enters into the formation of the spindle.
[FIG. 25. OVUM OF ASTERIAS GLACIALIS, AT THE SAME STAGE AS FIG. 24, TREATED WITH PICRIC ACID (copied from Fol).]
The following is Hertwig's (No. 92) account of the changes in the germinal vesicle in Asteracanthion. Shortly after the egg is laid the protoplasm on the side of the germinal vesicle towards the surface of the egg develops a prominence which presses inwards the wall of the vesicle. At the same time the germinal spot develops a large vacuole, in the interior of which is a body consisting of nuclear substance, and formed of a firmer and more refractive material than the remainder of the germinal spot. In the prominence first mentioned as projecting inwards towards the germinal vesicle first one star, formed by radial striæ of protoplasm, and then a second make their appearance; while the germinal spot appears to have vanished, the outline of the germinal vesicle to have become indistinct, and its contents to have mingled with the surrounding protoplasm. Treatment with reagents demonstrates that in the process of disappearance of the germinal spot the nuclear mass in its vacuole forms a rod-like body, the free end of which is situated between the two stars which occupy the prominence indenting the germinal vesicle. At a later period granules may be seen at the end of the rod and finally the rod itself vanishes. After these changes by the aid of reagents there may be demonstrated a spindle between the two stars, which Hertwig believes to grow in size as the last remnants of the germinal spot gradually vanish, and he maintains that the spindle is formed at the expense of the germinal spot. The stage with this spindle corresponds with fig. 25.
Several of Hertwig's figures closely correspond with those of Fol, and considering how conflicting is the evidence before us, it seems necessary to leave open for Asterias the question as to what parts of the germinal vesicle are concerned in forming the first spindle.
A clearer view of the phenomena which take place at this stage has been obtained by Fol in the case of Heteropods (Pterotrachæa). In the ovum a few minutes after it has been laid the germinal vesicle becomes very pale, and two stars make their appearance round a clear substance near its poles. The nucleus itself is somewhat elongated, and commences to exhibit at its poles longitudinal striæ, which gradually extend towards the centre at the expense of the nuclear reticulum, from a metamorphosis of which they are directly derived. When the striæ of the two sides have nearly met, thickenings may be observed in the recticulum between them, which give rise, where the striæ of the two sides unite, to the central thickenings of the fibres (nuclear plate). In this way a complete nuclear spindle is established[29].
[29] For the further details on the nuclear spindle vide the next Chapter.
The important result of Fol's observations on Heteropods, which tallies also with what is found in Asterias, is that a spindle with two stars at its poles is formed from the metamorphosis of the germinal vesicle and surrounding protoplasm (fig. 25).
[FIG. 26. PORTION OF THE OVUM OF ASTERIAS GLACIALIS AT THE MOMENT OF THE DETACHMENT OF THE FIRST POLAR BODY AND THE WITHDRAWAL OF THE REMAINING PART OF THE SPINDLE WITHIN THE OVUM. PICRIC ACID PREPARATION (copied from Fol).]
Polar cells. The spindle has up to this time been situated with its axis parallel to the surface of the egg, but in somewhat older specimens a vertical spindle is found, with one end projecting into a protoplasmic prominence which makes its appearance on the surface of the egg (fig. 26). Hertwig believes that the spindle simply travels towards the surface, and while doing so changes the direction of its axis. Fol asserts, however, that this is not the case, but that between the two phases of the spindle an intermediate one is found in which a spindle can no longer be seen in the egg, but its place is taken by a body with a dentated outline. He has not been able to arrive at a conclusion as to what meaning is to be attached to this occurrence, which does not appear to take place in Heteropods.
[FIG. 27. PORTION OF THE OVUM OF ASTERIAS GLACIALIS, WITH THE FIRST POLAR CELL AS IT APPEARS WHEN LIVING (copied from Fol).]
In any case the spindle which projects into the prominence on the surface of the egg divides into two parts, one in the prominence and one in the egg (fig. 26). The prominence itself with the enclosed portion of the spindle becomes constricted off from the egg to form a body, well known to embryologists as the polar body or cell (fig. 27). Since more than one polar cell is formed, that which is the earliest to appear may be called the first polar cell.
[FIG. 28. PORTION OF THE OVUM OF ASTERIAS GLACIALIS IMMEDIATELY AFTER THE FORMATION OF THE SECOND POLAR CELL. PICRIC ACID PREPARATION (copied from Fol).]
The part of the spindle which remains in the egg becomes directly converted into a second spindle by the elongation of its fibres, without passing through a typical nuclear condition. A second polar cell next becomes formed in the same manner as the first (fig. 28), and the portion of the spindle remaining in the egg becomes converted into two or three clear vesicles (fig. 29), which soon unite to form a single nucleus (fig. 30). The new nucleus which is clearly derived from part of the original germinal vesicle is called the female pronucleus, for reasons which will appear in the sequel.
[FIG. 29. PORTION OF THE OVUM OF ASTERIAS GLACIALIS AFTER THE FORMATION OF THE SECOND POLAR CELL, SHEWING THE PART OF THE SPINDLE REMAINING IN THE OVUM BECOMING CONVERTED INTO TWO CLEAR VESICLES. PICRIC ACID PREPARATION (copied from Fol).]
The two polar cells appear to be situated between two membranes, the outer of which is very delicate, and only distinct where it covers the polar cells, while the inner one is thicker and becomes, after impregnation, more distinct, and then forms what Fol speaks of as the vitelline membrane. It is clear, as Hertwig has pointed out, that the polar bodies originate by a regular process of cell division and have the value of cells.
A peculiar phenomenon makes its appearance in the eggs of Clepsine shortly after the formation of the polar cells, which has been spoken of by Whitman (No. 100) as the formation of the polar rings. The following is his description of the occurrence.
"Fifteen minutes after the elimination of the polar globules (i.e. cells) a ring-like depression or constriction appears in the yolk around the oral pole, and in this depression a transparent liquid substance (nuclear?) is collected forming the first polar ring.... The same phenomena repeat themselves later at the aboral pole.... The rings concentrate to form two discs.... Before the first cleavage both discs plunge deep into the egg."
The nature of these rings is at present quite obscure.
[FIG. 30. OVUM OF ASTERIAS GLACIALIS WITH THE TWO POLAR CELLS AND THE FEMALE PRONUCLEUS SURROUNDED BY RADIAL STRIÆ, AS SEEN IN THE LIVING EGG (copied from Fol).]
Considering how few ova have been adequately investigated with reference to the behaviour of the germinal vesicle, any general conclusions which may at present be formed are to be regarded as provisional.
There is however abundant evidence that at the time of maturation of the egg the germinal vesicle undergoes peculiar changes, which are, in part at least, of a retrogressive character. These changes may begin considerably before the egg has reached the period of maturity, or may not take place till after it has been laid. They consist in an appearance of irregularity and obscurity in the outline of the germinal vesicle, the absorption of its membrane, the partial absorption of its contents in the yolk, the disappearance of the reticulum, and the breaking up and disappearance of the germinal spot. The exact fate of the single germinal spot, or the numerous spots where they are present, is still obscure.
The retrogressive metamorphosis of the germinal vesicle is followed in a large number of instances by the conversion of what remains into a striated spindle similar in character to a nucleus previous to division. This spindle travels to the surface of the ovum and undergoes division to form the polar cell or cells in the manner above described. The part which remains in the egg forms eventually the female pronucleus.
The germinal vesicle has up to the present time only been observed to undergo the above series of changes in a certain number of instances, which, however, include examples from several divisions of the Coelenterata, the Echinodermata, and the Mollusca, some of the Vermes [Turbellarians (Leptoplana), Nematodes, Hirudinea, Alciope, Sagitta], Ascidians, etc. It is very possible, not to say probable, that such changes are universal in the animal kingdom, but the present state of our knowledge does not justify us in saying so.
In the Craniata especially our knowledge of the formation of the polar bodies is very unsatisfactory. In Petromyzon Kupffer and Benecke have brought forward evidence to shew that one polar body is formed prior to the impregnation, and a second in connection with a peculiar prominence of protoplasm after impregnation. Part of the germinal vesicle remains in the egg as the female pronucleus. In the Sturgeon the germinal vesicle atrophies and breaks up before impregnation, and afterwards part is found as a granular mass on the surface of the egg, while part forms a female pronucleus.
In Amphibia the observations of Hertwig (90) and Bambeke (77) tend to shew that after the germinal vesicle has assumed a superficial situation at the pigmented pole of the ovum its contents become intermingled with the yolk, and are in part extruded from the ovum as a granular mass after impregnation. Part of them remains in the ovum and forms a female pronucleus. Whether there is a proper division of the germinal vesicle as in typical cases is not known.
Oellacher (95) by a series of careful observations upon the egg of the trout, and subsequently of the bird, demonstrated that in the ovum while still in the ovary, the germinal vesicle underwent a kind of degeneration and eventually became ejected, in part at any rate. My own observations on Elasmobranchs, which require enlargement and confirmation, tend to shew that this part may be the membrane. Ed. van Beneden (78) has contributed some important observations on the rabbit. His account is as follows. As the ovum approaches maturity the germinal vesicle assumes an eccentric position, and fuses with the peripheral layer of the egg to constitute the cicatricular lens. The germinal spot next travels to the surface of the cicatricular lens and forms the nuclear disc: at the same time the membrane of the germinal vesicle vanishes, though it probably unites with the nuclear disc. The plasma of the nucleus then collects into a definite mass and forms the nucleoplasmic body. Finally the nuclear disc assumes an ellipsoidal form and becomes the nuclear body. Nothing is now left of the original germinal vesicle but the nuclear body and the nucleoplasmic body, both still situated within the ovum. In the next stage no trace of the germinal vesicle can be detected in the ovum, but outside it, close to the point where the modified remnants of the vesicle were previously situated, there is present a polar body which is composed of two parts, one of which stains deeply and resembles the nuclear body, and the other does not stain but is similar to the nucleoplasmic body. Van Beneden concludes that the parts of the polar body are the two ejected products of the germinal vesicle. We may be perhaps permitted to hold that further observations on this difficult object will demonstrate that part of the germinal vesicle remains in the ovum to form the female pronucleus.
With reference to invertebrate forms attention may be called to the observations of Bütschli (80). Although in Cucullanus a normal formation of the polar bodies takes place, yet in the Nematodes generally, Bütschli has been unable to find the spindle modification of the germinal vesicle, but states that the germinal vesicle undergoes degeneration, its outline becoming indistinct and the germinal spot vanishing. The position of the germinal vesicle continues to be marked by a clear space, which gradually approaches the surface of the egg. When it is in contact with the surface a small spherical body, the remnant of the germinal vesicle, comes into view, and eventually becomes ejected. The clear space subsequently disappears.
In addition to the types just quoted, which may very probably turn out to be normal in the mode of formation of the polar bodies, there is a large number of types, including the whole of the Rotifera and Arthropoda with a few doubtful exceptions[30], in which the polar cells cannot as yet be said to have been satisfactorily observed.
[30] The best instance of what appears like a polar cell in Arthropoda is a body recently found by Grobben ("Entwicklungsgeschichte d. Moina rectirostris." Claus' Arbeiten, Vol. II., Wien, 1879) near the surface of the protoplasm at the animal pole of the summer and parthenogenetic eggs of Moina rectirostris, one of the Cladocera. The body stains deeply with carmine, but differs from normal polar cells in not being separated from the ovum; and its identification as a polar cell must remain doubtful till it has been shewn to originate from the germinal vesicle.
The more important of the doubtful cases amongst the Rotifera and Arthropoda are the following.
Flemming (83) finds that in the summer and probably parthenogenetic eggs of Lacinularia socialis the germinal vesicle approaches the surface and becomes invisible, and that subsequently a slight indentation in the outline of the egg marks the point of its disappearance. In the hollow of the indentation Flemming believes a polar cell to be situated, though he has not definitely seen one.
Hoek[31] believes that he has found a polar body in the ovum of Balanus balanoides, but his observations are not perfectly satisfactory.
[31] "Zur Entwicklung d. Entomostraken." Niederlandischer Archiv. f. Zoologie, Vol. III. p. 62.
Bütschli, who has expressly searched for the polar bodies in the ova of Rotifera, was unable to find any trace of them, though he found that as the egg became ripe the germinal vesicle became half its original size. In the parthenogenetic eggs of Aphis he also failed to find a trace of polar bodies, though the germinal vesicle, after the germinal spot had broken up into fragments, approached the surface and disappeared.
Whatever may be the eventual result of more extended investigation, it is clear that the formation of polar cells according to the type described above is a very constant occurrence. Its importance is increased by the discovery by Strasburger of the existence of an analogous process amongst plants. Two questions about it obviously present themselves for solution: (1) What are the conditions of its occurrence with reference to impregnation? (2) What meaning has it in the development of the ovum or the embryo?
The answer to the first of these questions is not difficult to find. The formation of the polar bodies is independent of impregnation, and is the final act of the normal growth of the ovum. In a few types the polar cells are formed while the ovum is still in the ovary, as, for instance, in some species of Echini, Hydra, etc., but, according to our present knowledge, far more usually after the ovum has been laid. In some instances the budding-off of the polar cells precedes, and in other instances follows impregnation; but there is no evidence to shew that in the latter cases the process is influenced by the contact with the male element. In Asterias, as has been shewn by O. Hertwig and Fol, the formation of the polar cells may indifferently either precede or follow impregnation--a fact which affords a clear demonstration of the independence of the two occurrences.
To the second of the two questions it does not unfortunately seem possible at present to give an answer which can be regarded as satisfactory.
The retrogressive changes in the membrane of the germinal vesicle which usher in the formation of the polar bodies may very probably be viewed as a prelude to a renewed activity of the contents of the vesicle; and are perhaps rendered the more necessary from the thickness of the membrane which results from a protracted period of passive growth. This suggestion does not, however, help us to explain the formation of polar bodies by a process identical with cell division. The ejection of part of the germinal vesicle in the formation of the polar cells may probably be paralleled by the ejection of part or the whole of the original nucleus which, if we may trust the beautiful researches of Bütschli, takes place during conjugation in Infusoria as a preliminary to the formation of a fresh nucleus. This comparison is due to Bütschli, and according to it the formation of the polar bodies would have to be regarded as assisting, in some as yet unknown way, the process of regeneration of the germinal vesicle. Views analogous to this are held by Strasburger and Hertwig, who regard the formation of the polar bodies in the light of a process of excretion or removal of useless material. Such hypotheses do not, unfortunately, carry us very far.
I would suggest that in the formation of the polar cells part of the constituents of the germinal vesicle, which are requisite for its functions as a complete and independent nucleus, is removed, to make room for the supply of the necessary parts to it again by the spermatic nucleus.
My view amounts to the following, viz. that after the formation of the polar cells the remainder of the germinal vesicle within the ovum (the female pronucleus) is incapable of further development without the addition of the nuclear part of the male element (spermatozoon), and that if polar cells were not formed parthenogenesis might normally occur. A strong support for this hypothesis would be afforded were it to be definitely established that a polar body is not formed in the Arthropoda and Rotifera; since the normal occurrence of parthenogenesis is confined to these two groups. It is certainly a remarkable coincidence that they are the only two groups in which polar bodies have not so far been satisfactorily observed.
It is perhaps possible that the part removed in the formation of the polar cells is not absolutely essential; and this seems at first sight to follow from the fact of parthenogenesis being possible in instances where impregnation is the normal occurrence. The genuineness of the observations on this head is too long a subject to enter into here[32], but after admitting, as we probably must, that there are genuine cases of such parthenogenesis, it cannot be taken for granted without more extended observation that the occurrence of development in these rare instances may not be due to the polar cells not having been formed as usual, and that when the polar cells are formed the development without impregnation is impossible.
[32] The instances quoted by Siebold, Parthenogenesis d. Arthropoden, are not quite satisfactory. In Hensen's case, p. 234, impregnation would have been possible if we can suppose the spermatozoa to be capable of passing into the body cavity through the open end of the uninjured oviduct; and though Oellacher's instances are more valuable, yet sufficient care seems hardly to have been taken, especially when it is not certain for what length of time spermatozoa may be able to live in the oviduct. For Oellacher's precautions, vide Zeit. für Wiss. Zool., Bd. xxii., p. 202. A better instance is that of a sow given by Bischoff, Ann. Sci. Nat., series 3, Vol. II., 1844. The unimpregnated eggs were found divided into segments, but the segments did not contain the usual nucleus, and were perhaps nothing else than the parts of an ovum in a state of disruption.
Selenka found in the case of Purpura lapillus that no polar body was formed in the eggs which did not develop, but in the case of Neritina, Bütschli has found that this does not hold good.
The remarkable observations of Greeff (No. 88) on the parthenogenetic development of the eggs of Asterias rubens tell, however, very strongly against the above hypothesis. Greeff has found that under normal circumstances the eggs of this species of starfish will develop without impregnation in simple sea-water. The development is quite regular and normal, though much slower than in the case of impregnated eggs. It is not definitely stated that polar cells are formed, but there can be no doubt that this is implied. Greeff's account is so precise and circumstantial that it is not easy to believe that any error can have crept in; but neither Hertwig nor Fol have been able to repeat his experiments, and we may be permitted to wait for further confirmation before absolutely accepting them.
To the suggestion already made with reference to the function of the polar cells, I will venture to add the further one, that the function of forming polar cells has been acquired by the ovum for the express purpose of preventing parthenogenesis.
The explanation given by Mr Darwin of the evil effects of self-fertilization, viz. the want of sufficient differentiation in the sexual elements[33], would apply with far greater force to cases of parthenogenesis.
[33] Darwin, Cross- and Self-Fertilization of Plants, p. 443.
In the production of fresh individuals, two circumstances are obviously favourable to the species. (1) That the maximum number possible of fresh individuals should be produced, (2) That the individuals should be as vigorous as possible. Sexual differentiation (even in hermaphrodites) is clearly very inimical to the production of the maximum number of individuals. There can be little doubt that the ovum is potentially capable of developing by itself into a fresh individual, and therefore, unless the absence of sexual differentiation was very injurious to the vigour of the progeny, parthenogenesis would most certainly be a very constant occurrence; and, on the analogy of the arrangements in plants to prevent self-fertilization, we might expect to find some contrivance both in animals and in plants to prevent the ovum developing by itself without fertilization. If my view about the polar cells is correct, the formation of these bodies functions as such a contrivance.
Reproduction by budding or fission has probably arisen as a means of increasing the number of individuals produced, so that the coexistence of asexual with sexual reproduction is to be looked on as a kind of compromise for the loss of the power of rapid reproduction due to the absence of parthenogenesis. In the Arthropoda and Rotifera the place of budding has been taken by parthenogenesis, which may be a frequent, though not always a necessary occurrence, as in various Branchiopoda (Apus, Limnadia, etc.) and Lepidoptera (Psyche helix, etc.); or a regular occurrence for the production of one sex, as in Bees, Wasps, Nematus, etc.; or an occurrence confined to a certain stage in the cycle of development in which all the individuals reproduce their kind parthenogenetically, as in Aphis, Cecidomyia, Gall Insects (Neuroterus, etc.), Daphnia[34].
[34] Mr J. A. Osborne has recently shewn (Nature, Sept. 4, 1879), that the eggs of a Beetle (Gastrophysa raphani) may occasionally develop, up to a certain point at any rate, without the male influence.
On my hypothesis the possibility of parthenogenesis, or at any rate its frequency, in Arthropoda and Rotifera is possibly due to the absence of polar cells. In the case of all animals, so far as is known to me, fertilization of the ovum occasionally occurs[35], but there are instances in the vegetable kingdom where so-called parthenogenesis appears to be capable of recurring for an indefinite period. One of the best instances appears to be that of Coelebogyne, an introduced exotic Euphorbiaceous plant which regularly produces fertile seeds although a male flower never appears. The recent researches of Strasburger have however shewn that in Coelebogyne and other parthenogenetic flowering plants, embryos are formed by the budding and subsequent development of cells belonging to the ovule. This being the case, it is impossible to assert of these plants that they are really parthenogenetic, for the embryos contained in the seed of a flower which has certainly not been fertilized, may have been formed, not by the development of the ovum, but by budding from the surrounding tissue of the ovule.
[35] Dicyema, which is an apparent exception, has not yet been certainly shewn to develop true ova. If its germs are true ova it forms an exception to the above rule.
The above view with reference to the nature of the polar bodies is not to be regarded as forming more than an hypothesis.
Impregnation of the Ovum.
A far greater amount of certainty has been attained as to the effects of impregnation than as to the changes of the germinal vesicle which precede this, and there appears, moreover, to be a greater uniformity in the series of resulting phenomena.
[FIG. 31. SMALL PORTIONS OF THE OVUM OF ASTERIAS GLACIALIS. THE SPERMATOZOA ARE SHEWN ENVELOPED IN THE MUCILAGINOUS COAT. IN A. A PROMINENCE IS RISING FROM THE SURFACE OF THE EGG TOWARDS THE NEAREST SPERMATOZOON; AND IN B. THE SPERMATOZOON AND PROMINENCE HAVE MET. (Copied from Fol.)]
[FIG. 32. PORTION OF THE OVUM OF ASTERIAS GLACIALIS AFTER THE ENTRANCE OF A SPERMATOZOON INTO THE OVUM. IT SHEWS THE PROMINENCE OF THE OVUM THROUGH WHICH THE SPERMATOZOON HAS ENTERED. A VITELLINE MEMBRANE WITH A CRATER-LIKE OPENING HAS BECOME DISTINCTLY FORMED. (Copied from Fol.)]
It will be convenient again to take Asterias glacialis as the type. The part of the germinal vesicle which remains in the egg, after the formation of the second polar cell, becomes converted into a number of small vesicles (fig. 29), which aggregate themselves into a single clear nucleus, which gradually travels toward the centre of the egg and around which, as a centre, the protoplasm becomes radiately striated (fig. 30). This nucleus is known as the female pronucleus. By the action of reagents a nucleolus may be shewn in it. In Asterias glacialis the most favourable period for fecundation is about an hour after the formation of the female pronucleus. If at this time the spermatozoa are allowed to come in contact with the egg, their heads soon become enveloped in the investing mucilaginous coat. A prominence, pointing towards the nearest spermatozoon, now arises from the superficial layer of protoplasm of the egg, and grows till it comes in contact with the spermatozoon (fig. 31, A and B). Under normal circumstances the spermatozoon which meets the prominence is the only one concerned in the fertilization, and it makes its way into the egg by passing through the prominence. The tail of the spermatozoon, no longer motile, remains visible for some time after the head has bored its way in, but its place is soon taken by a pale conical body, which is, however, probably in part a product of the metamorphosis of the tail itself (fig. 32). It eventually becomes absorbed into the body of the ovum.
At the moment of contact between the spermatozoon and the egg the outermost layer of the protoplasm of the latter raises itself as a distinct membrane, which separates from the egg and prevents the entrance of other spermatozoa. At the point where the spermatozoon entered a crater-like opening is left in the membrane, through which the metamorphosed tail of the spermatozoon may at first be seen projecting (fig. 32).
[FIG. 33. OVUM OF ASTERIAS GLACIALIS, WITH MALE AND FEMALE PRONUCLEUS AND A RADIAL STRIATION OF THE PROTOPLASM AROUND THE FORMER. (Copied from Fol.)]
The head of the spermatozoon when in the egg forms a nucleus, for which the name male pronucleus may be conveniently adopted. It grows in size, probably by assimilating material from the ovum, and around it is formed a clear space free from yolk-spherules. Shortly after its formation the protoplasm in its neighbourhood assumes a radiate arrangement (fig. 33). At whatever point of the egg the spermatozoon may have entered, it gradually travels towards the female pronucleus. The latter, around which the protoplasm no longer has a radiate arrangement, remains motionless till the rays of the male pronucleus come in contact with it, after which its condition of repose is exchanged for one of activity, and it rapidly approaches the male pronucleus, apparently by means of its inherent amoeboid contractions, and eventually fuses with it (figs. 34-36).
As the male pronucleus approaches the female the latter, according to Selenka, sends out protoplasmic processes which embrace the former. The actual fusion does not take place till after the pronuclei have been in contact for some time. While the two pronuclei are approaching one another the protoplasm of the egg exhibits amoeboid movements.
[FIGS. 34, 35, AND 36. THREE SUCCESSIVE STAGES IN THE COALESCENCE OF THE MALE AND FEMALE PRONUCLEI IN ASTERIAS GLACIALIS. FROM THE LIVING OVUM. (Copied from Fol.)]
The product of the fusion of the two pronuclei forms the first segmentation nucleus (fig. 37), which soon, however, divides into the two nuclei of the two first segmentation spheres.
[FIG. 37. OVUM OF ASTERIAS GLACIALIS, AFTER THE COALESCENCE OF THE MALE AND FEMALE PRONUCLEI. (Copied from Fol.)]
The phenomenon which has just been described consists essentially in the fusion of the male cell and the female cell. In this act the protoplasm of the two cells as well as their nuclei coalesce, since the whole spermatozoon which has been absorbed into the ovum is a cell of which the head is the nucleus.
It is clear that the ovum after fertilization is an entirely different body to the ovum prior to that act, and unless the use of the same term for the two conditions of the ovum had become very familiar, a special term, such as oosperm, for the ovum after its fusion with the spermatozoon, would be very convenient.
Of the earlier observations on this subject there need perhaps only be cited one of E. van Beneden, on the rabbit's ovum, shewing the presence of two nuclei before the commencement of segmentation. Bütschli was the earliest to state from observations on Rhabditis dolichura that the first segmentation nucleus arose from the fusion of two nuclei, and this was subsequently shewn with greater detail for Ascaris nigrovenosa, by Auerbach (76). Neither of these authors gave at the first the correct interpretation of their results. At a later period Bütschli (80) arrived at the conclusion that in a large number of instances (Lymnæus, Nephelis, Cucullanus, &c.), the nucleus in question was formed by the fusion of two or more nuclei, and Strasburger at first made a similar statement for Phallusia, though he has since withdrawn it. Though Bütschli's statements depend, as it seems, upon a false interpretation of appearances, he nevertheless arrived at a correct view with reference to what occurs in impregnation. Van Beneden (78) described in the rabbit the formation of the original segmentation nucleus from two nuclei, one peripheral and the other central, and deduced from his observations that the peripheral nucleus was derived from the spermatic element. It was reserved for Oscar Hertwig (89) to describe in Echinus lividus the entrance of a spermatozoon into the egg and the formation from it of the male pronucleus.
The general fact that impregnation consists in the fusion of the spermatozoon and ovum has now been established for some forms in the majority of invertebrate groups (Arthropoda and Rotifera excepted). Amongst Vertebrata also it has been shewn by E. van Beneden that the first segmentation nucleus is formed by the coalescence of the male and female pronucleus. Calberla, and Kupffer and Benecke have demonstrated that a single spermatozoon enters at first the ovum of Petromyzon.
The contact of the spermatozoon with the egg membrane causes in Petromyzon active movements of the protoplasm of the ovum, and a retreat of the protoplasm from the membrane.
In Amphibia the appearance of a peculiar pigmented streak extending inwards from the surface of the pigmented pole of the ovum, and containing in a clear space at its inner extremity a nucleus, has been demonstrated as the result of impregnation by Bambeke (77) and Hertwig (90). There can be little doubt that this nucleus is the male pronucleus, and that the pigmented streak indicates its path inwards. Close to it Hertwig has shewn that another nucleus is to be found, the female pronucleus, and that eventually the two join together. In Amphibia the phenomena accompanying impregnation are clearly of the same nature as in the Invertebrata. A precisely similar series of phenomena to those in Amphibia has been shewn by Salensky to take place in the Sturgeon.
Although there is a general agreement between the most recent observers, Hertwig, Fol, Selenka, Strasburger, &c., as to the main facts connected with the entrance of one spermatozoon into the egg, the formation of the male pronucleus, and its fusion with the female pronucleus, there still exist differences of detail in the different descriptions, which partly, no doubt, depend upon the difficulties of observation, but partly also upon the observations not having all been made upon the same species. Hertwig does not enter into details with reference to the actual entrance of the spermatozoon into the egg, but in his latest paper points out that considerable differences may be observed in the occurrences which succeed impregnation, according to the relative period at which this takes place. When, in Asterias, the impregnation is effected about an hour after the egg is laid, and previously to the formation of the polar cells, the male pronucleus appears at first to exert but little influence on the protoplasm, but after the formation of the second polar cell, the radial striæ around it become very marked, and the pronucleus rapidly grows in size. When it finally unites with the female pronucleus it is equal in size to the latter. In the case when the impregnation is deferred for four hours the male pronucleus never becomes so large as the female pronucleus. With reference to the effect of the time at which impregnation takes place, Asterias would seem to serve as a type. Thus in Hirudinea, Mollusca, and Nematoidea impregnation normally takes place before the formation of the polar bodies is completed, and the male pronucleus is accordingly as large as the female. In Echinus, on the other hand, where the polar bodies are formed in the ovary, the male pronucleus is always small.
Selenka, who has investigated the formation of the male pronucleus in Toxopneustes variegatus, differs in certain points from Fol. He finds that usually, though not always, a single spermatozoon enters the egg, and that though the entrance may be effected at any part of the surface it generally occurs at the point marked by a small prominence where the polar cells are formed. The spermatozoon first makes its way through the mucous envelope of the egg, within which it swims about, and then bores with its head into the polar prominence.
One important point has been so far only indirectly alluded to, viz. the number of spermatozoa required to effect impregnation.
The concurrent testimony of almost all observers tends to shew that one only is required for this purpose. But the number of cases tested is too small to admit of satisfactory generalization.
Both Hertwig and Fol have made observations on the result of the entrance into the egg of several spermatozoa. Fol finds that when the impregnation has been too long delayed the vitelline membrane is formed with comparative slowness, and several spermatozoa are thus enabled to penetrate. Each spermatozoon forms a separate pronucleus with a surrounding star; and several male pronuclei usually fuse with the female pronucleus. Each male pronucleus appears to exercise a repulsive influence on other male pronuclei, but to be attracted by the female pronucleus. When there are several male pronuclei the segmentation is irregular and the resulting larva a monstrosity. These statements of Fol and Hertwig are up to a certain point in contradiction with the more recent results of Selenka. In Toxopneustes variegatus Selenka finds that though impregnation is usually effected by a single spermatozoon yet several may be concerned in the act. The development continues, however, to be normal up to the gastrula stage, at any rate, if three or even four spermatozoa enter the egg almost simultaneously. Under such circumstances each spermatozoon forms a separate pronucleus and star. Selenka is of opinion (apparently rather on a priori grounds than as a result of direct observation) that normal development cannot occur when more than one male pronucleus fuses with the female pronucleus; and holds that, where he has observed such normal development after the entrance of more than one spermatozoon, the majority of male pronuclei become absorbed.
It may be noticed that, while the observations of Fol and Hertwig were admittedly made upon eggs in which the impregnation was delayed till they no longer displayed their pristine activity, Selenka's were made upon quite fresh eggs; and it seems not impossible that the pathological symptoms in the embryos reared by the two former authors may have been due to the imperfection of the egg, and not to the entrance of more than one spermatozoon. This, of course, is merely a suggestion which requires to be tested by fresh observations.
Kupffer and Benecke have further shewn that although only one spermatozoon enters the ovum directly in Petromyzon yet other spermatozoa pass through the vitelline membrane, and are taken into a peculiar protoplasmic protuberance of the ovum which appears after impregnation.
The act of impregnation may be described as the fusion of the ovum and spermatozoon, and the most important feature in this act appears to be the fusion of a male and female nucleus; not only does this appear in the actual fusion of the two pronuclei, but it is brought into still greater prominence by the fact that the female pronucleus is a product of the nucleus of a primitive ovum, and the male pronucleus is the metamorphosed head of the spermatozoon which, as stated above, contains part of the nucleus of the primitive spermatic cell. The spermatic cells originate from cells indistinguishable from the primitive ova, so that the fusion which takes place is the fusion of morphologically similar parts in the two sexes.
These conclusions tally very satisfactorily with the view adopted in the Introduction, that impregnation amongst the Metazoa was derived from the process of conjugation amongst the Protozoa.
Summary.
In what may probably be regarded as a normal case the following series of events accompanies the maturation and impregnation of an ovum:--
(1) Transportation of the germinal vesicle to the surface of the egg.
(2) Absorption of the membrane of the germinal vesicle and metamorphosis of the germinal spot and nuclear reticulum.
(3) Assumption of a spindle character by the remains of the germinal vesicle, these remains being probably in part formed from the germinal spot.
(4) Entrance of one end of the spindle into a protoplasmic prominence at the surface of the egg.
(5) Division of the spindle into two halves, one remaining in the egg, the other in the prominence; the prominence becoming at the same time nearly constricted off from the egg as a polar cell.
(6) Formation of a second polar cell in the same manner as the first, part of the spindle still remaining in the egg.
(7) Conversion of the part of the spindle remaining in the egg into a nucleus--the female pronucleus.
(8) Transportation of the female pronucleus towards the centre of the egg.
(9) Entrance of one spermatozoon into the egg.
(10) Conversion of the head of the spermatozoon into a nucleus--the male pronucleus.
(11) Appearance of radial striæ round the male pronucleus, which gradually travels towards the female pronucleus.
(12) Fusion of male and female pronuclei to form the first segmentation nucleus.
(76) Auerbach. Organologische Studien, Heft 2. Breslau, 1874.
(77) Bambeke. "Recherches s. Embryologie des Batraciens." Bull. de l'Acad. royale de Belgique, 2me Sér., T. LXI., 1876.
(78) E. van Beneden. "La Maturation de l'OEuf des Mammifères." Bull. de l'Acad. royale de Belgique, 2me Sér., T. XL. No. 12, 1875.
(79) Idem. "Contributions à l'Histoire de la Vésicule Germinative, &c." Bull. de l'Acad. royale de Belgique, 2me Sér., T. XLI. No. 1, 1876.
(80) O. Bütschli. Eizelle, Zelltheilung, und Conjugation der Infusorien. Frankfurt, 1876.
(81) F. M. Balfour. "On the Phenomena accompanying the Maturation and Impregnation of the Ovum." Quart. J. of Micros. Science, Vol. XVIII., 1878.
(82) Calberla. "Befruchtungsvorgang beim Ei von Petromyzon Planeri." Zeit. f. wiss. Zool., Vol. XXX.
(83) W. Flemming. "Studien in d. Entwickelungsgeschichte der Najaden." Sitz. d. k. Akad. Wien, B. LXXI., 1875.
(84) H. Fol. "Die erste Entwickelung des Geryonideneies." Jenaische Zeitschrift, Vol. VII., 1873.
(85) Idem. "Sur le Développement des Ptéropodes." Archives de Zoologie Expérimentale et Générale, Vol. IV. and V., 1875-6.
(86) Idem. "Sur le Commencement de l'Hénogénie." Archives des Sciences Physiques et Naturelles. Genève, 1877.
(87) Idem. Recherches s. l. Fécondation et l. commen. d. l'Hénogénie. Genève, 1879.
(88) R. Greeff. "Ueb. d. Bau u. d. Entwickelung d. Echinodermen." _Sitzun. der Gesellschaft z. Beförderung d. gesammten Naturwiss. z. Marburg_, No. 5, 1876.
(89) Oscar Hertwig. "Beit. z. Kenntniss d. Bildung, &c., d. thier. Eies." Morphologisches Jahrbuch, Vol. I., 1876.
(90) Idem. Ibid. Morphologisches Jahrbuch, Vol. III. Heft 1, 1877.
(91) Idem. "Weitere Beiträge, &c." Morphologisches Jahrbuch, Vol. III., 1877, Heft 3.
(92) Idem. "Beit. z. Kenntniss, &c." Morphologisches Jahrbuch, Vol. IV. Heft 1 and 2, 1878.
(93) N. Kleinenberg. Hydra. Leipzig, 1872.
(94) C. Kupffer u. B. Benecke. Der Vorgang d. Befruchtung am Eie d. Neunaugen. Königsberg, 1878.
(95) J. Oellacher. "Beiträge zur Geschichte des Keimbläschens im Wirbelthiere." Archiv f. mikr. Anat., Bd. VIII., 1872.
(96) W. Salensky. "Befruchtung u. Furchung d. Sterlets-Eies." Zoologischer Anzeiger, No. 11, 1878.
(97) E. Selenka. Befruchtung des Eies von Toxopneustes variegatus. Leipzig, 1878.
(98) Strasburger. Ueber Zellbildung u. Zelltheilung. Jena, 1876.
(99) Idem. Ueber Befruchtung u. Zelltheilung. Jena, 1878.
(100) C. O. Whitman. "The Embryology of Clepsine." Quart. J. of Micr. Science, Vol. XVIII., 1878.