The Works of Francis Balfour 3-13

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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Cephalochorda | Urochorda | Elasmobranchii | Teleostei | Cyclostomata | Ganoidei | Amphibia | Aves | Reptilia | Mammalia | Comparison of the Formation of Germinal Layers and Early Stages in Vertebrate Development | Ancestral form of the Chordata | General Conclusions | Epidermis and Derivatives | The Nervous System | Organs of Vision | Auditory, Olfactory, and Lateral Line Sense Organs | Notochord, Vertebral Column, Ribs, and Sternum | The Skull | Pectoral and Pelvic Girdles and Limb Skeleton | Body Cavity, Vascular System and Glands | The Muscular System | Excretory Organs | Generative Organs and Genital Ducts | The Alimentary Canal and Appendages in Chordata
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This historic 1885 book edited by Foster and Sedgwick is the third of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.
Modern Notes:

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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Vol. III. A Treatise on Comparative Embryology 2 (1885)



IT has already been shewn in the earlier chapters of the work that during the first phases of development the history of all the Metazoa is the same. They all originate from the coalescence of two cells, the ovum and spermatozoon. The coalesced product of these cells the fertilized ovum then undergoes a process known as the segmentation, in the course of which it becomes divided in typical cases into a number of uniform cells. An attempt was made from the point of view of evolution to explain these processes. The ovum and spermatozoon were regarded as representing phylogenetically two physiologically differentiated forms of a Protozoon ; their coalescence was equivalent to conjugation : the subsequent segmentation of the fertilized ovum was the multiplication by division of the organism resulting from the conjugation ; the resulting organisms, remaining, however, united to form a fresh organism in a higher state of aggregation.

In the systematic section of this work the embryological history of the Metazoa has been treated. The present chapter contains a review of the cardinal features of the various histories, together with an attempt to determine how far there are any points common to the whole of these histories ; and the phylogenetic interpretation to be given to such points.

Some years ago it appeared probable that a definite answer


would be given to the questions which must necessarily be raised in the present chapter ; but the results of the extended investigations made during the last few years have shewn that these expectations were premature, and in spite of the numerous recent valuable contributions to this branch of Embryology, amongst which special attention may be called to those of Kowalevsky (No. 277), Lankester (Nos. 278 and 279), and Haeckel (No. 266), there are few embryologists who would venture to assert that any answers which can be given are more than tentative gropings towards the truth.

In the following pages I aim more at summarising the facts, and critically examining the different theories which can be held, than at dogmatically supporting any definite views of my own.

In all the Metazoa, the development of which has been investigated, the first process of differentiation, which follows upon the segmentation, consists in the cells of the organism becoming divided into two groups or layers, known respectively as epiblast and hypoblast.

These two layers were first discovered in the young embryos of vertebrated animals by Pander and Von Baer, and have been since known as the germinal layers, though their cellular nature was not at first recognised. They were shewn, together with a third layer, or mesoblast, which subsequently appears between them, to bear throughout the Vertebrata constant relations to the organs which became developed from them. A very great step was subsequently made by Remak (No. 287), who successfully worked out the problem of vertebrate embryology on the cellular theory.

Rathke in his memoir on the development of Astacus (No. 286) attempted at a very early period to extend the doctrine of the derivation of the organs from the germinal layers to the Invertebrata. In 1859 Huxley made an important step towards the explanation of the nature of these layers by comparing them with the ectoderm and endoderm of the Hydrozoa ; while the brilliant researches of Kowalevsky on the development of a great variety of invertebrate forms formed the starting point of the current views on this subject.

The differentiation of the epiblast and hypoblast may commence during the later phases of the segmentation, but is generally not completed till after its termination. Not only do the cells of the blastoderm become differentiated



into two layers, but these very large number of

two layers, in the case of a ova with but little food-yolk, con

(fig. 198) the require further


(From Gegenbaur.)

a. mouth ; b. archenteron ; c. hypoblast ; d. epiblast.

stitute a double-walled sack the gastrula characters of which are too well known to description. Following the lines of phylogenetic speculation above indicated, it may be concluded that the two-layered condition of the organism represents in a general way the passage from the protozoon to the metazoon condition. It is probable that we may safely go further, and assert that the gastrula reproduces, with more or less fidelity, a stage in the evolution of the Metazoa, permanent in the simpler Hydrozoa, during which the organism was provided with (i) a fully developed digestive cavity (fig. 198 b) lined by the hypoblast with digestive and assimilative functions, (2) an oral opening (a), and (3) a superficial epiblast (d}. These generalisations, which are now widely accepted, are no doubt very valuable, but they leave unanswered the following important questions :

(1) By what steps did the compound Protozoon become differentiated into a Metazoon ?

(2) Are there any grounds for thinking that there is more than one line along which the Metazoa have become independently evolved from the Protozoa ?

(3) To what extent is there a complete homology between the two primary germinal layers throughout the Metazoa ?

Ontogenetically there is a great variety of processes by which the passage from the segmented ovum to the two-layered or diploblastic condition is arrived at.

These processes may be grouped under the following heads : 1. Invagination. Under this term a considerable number of closely connected processes are included. When the segmentation results in the formation of a blastosphere, one half of the blastosphere may be pushed in towards the opposite half, and a gastrula be thus produced (fig. 199, A and B). This process is known as embolic invagination. Another process, known as epibolic invagination, consists in epiblast cells growing round and en



closing the hypoblast (fig. 200). This process replaces the former process when the hypoblast cells are so bulky from being distended by food-yolk that their invagination is mechanically impossible.


VIEWED IN OPTICAL SECTION. (After Selenka.) A. Stage at the close of segmentation. B. Gastrula stage.

mr. micropyle ; fl. chorion ; s.c. segmentation cavity; bl. blastoderm; ep. epiblast; hy. hypoblast ; ms. amoeboid cells derived from hypoblast ; a.e. archenteron.

There are various peculiar modifications of invagination which cannot be dealt with in detail.

Invagination in one form or other occurs in some or all the members of the following groups :

The Dicyemidae, Calcispongiae (after the amphiblastula stage) and Silicispongiae, Coelenterata, Turbellaria, Nemertea, Rotifera, Mollusca, Polyzoa, Brachiopoda, Chaetopoda, Discophora, Gephyrea, Chaetognatha, Nematelminthes, Crustacea, Echinodermata, and Chordata.

The gastrula of the Crustacea is peculiar, as is also that of many of the Chordata (Reptilia, Aves, Mammalia), but there is every reason to suppose


ep. epiblast ; ms. mesoblastic band ; hy. hypoblast.



that the gastrulae of these groups are simply modifications of the normal type.

2. Delamination. Three types of delamination may be distinguished :

a. Delamination where the cells of a solid morula become divided into a superficial epiblast, and a central solid mass in which the digestive cavity is subsequently hollowed out (fig. 201).



A. Stage after the delamination; ep. epiblastic invagination to form pneumatocyst.

B. Later stage after the formation of the gastric cavity in the solid hypoblast. po. polypite ; /. tentacle ; pp. pneumatocyst ; ep. epiblast of pneumatocyst ; hy. hypoblast surrounding pneumatocyst.

b. Delamination where the segmented ovum has the form of a blastosphere, the cells of which give rise by budding to scattered cells in the interior of the vesicle, which, though they may at first form a solid mass, finally arrange themselves in the form of a definite layer around a central digestive cavity (fig. 202).

c. Delamination where the segmented ovum has the form of a blastosphere in the cells of which the protoplasm is differentiated into an inner and an outer part. By a subsequent



process the inner parts of the cells become separated from the outer, and the walls of the blastosphere are so divided into two distinct layers (fig. 205).

Although the third of these processes is usually regarded as the type of delamination, it does not, so far as I know, occur in nature, but is most nearly approached in Geryonia (fig. 203).

The first type of delamination is found in the Ceratospongiae, some Silicispongiae (?), and in many Hydrozoa and Actinozoa, and in Nemertea and Nematelminthes (Gordioidea ?). The second type occurs in many Porifera \Calcispongi(e (A see t fa), Myxospongice], and in some Coelenterata, and Brachiopoda ( Thecidium).

Delamination and invagination are undoubtedly the two most frequent modes in which the layers are differentiated, but


FIG. 202. THREE LARVAL STAGES OF EUCOPE POLYSTYLA. (After Kowalevsky.) A. Blastosphere stage with hypoblast spheres becoming budded off into central cavity. B. Planula stage with solid hypoblast. C. Planula stage with a gastric cavity, ep. epiblast ; hy. hypoblast ; al. gastric cavity.

there are in addition several others. In the first place the whole of the Tracheata (with the apparent exception of the Scorpion) develop, so far as is known, on a plan peculiar to them, which approaches delamination. This consists in the appearance of a superficial layer of cells enclosing a central yolk mass, which corresponds to the hypoblast (figs. 204 and 214). This mode of development might be classed under delamination, were it not for the fact that the early development



of many Crustacea is almost the same, but is subsequently followed by an invagination (fig. 208), which apparently corre



A. Stage at the commencement of the delamination ; the dotted lines x shew

the course of the next planes of division. B. Stage at the close of the delamination.

cs. segmentation cavity ; a. endoplasm ; b. ectoplasm ; ep. epiblast ; hy. hypoblast.

spends to the normal invagination of other types. There are strong grounds for thinking that the tracheate type of forma


(After Metschnikoff. )

In A the ovum is divided into a number of separate segments. In B a number of small cells have appeared (bl) which form a blastoderm enveloping the large yolkspheres. In C the blastoderm has become divided into two layers.

B. III. 22


tion of the epiblast and hypoblast is a secondary modification of an invaginate type (vide Vol. II. p. 457).

The type of some Turbellaria (Stylochopsis ponticus) and that of Nephelis amongst the Discophora is not capable of being reduced to the invaginate type.

The development of almost all the parasitic groups, i.e. the Trematoda, the Cestoda, the Acanthocephala, and the Linguatulida, and also of the Tardigrada, Pycnogonida, and other minor groups, is too imperfectly known to be classed with either the delaminate or invaginate types.

It will, I think, be conceded on all sides that, if any of the ontogenetic processes by which a gastrula form is reached are repetitions of the process by which a simple two-layered gastrula was actually evolved from a compound Protozoon, these processes are most probably of the nature either of invagination or of delamination.

The much disputed questions which have been raised about the gastrula and planula theories, originally put forward by Haeckel and Lankester, resolve themselves then into the simple question, whether any, and if so which, of the ontogenetic processes by which the gastrula is formed are repetitions of the phylogenetic origin of the gastrula.

It is very difficult to bring forward arguments of a conclusive kind in favour of either of these processes. The fact that delaminate and invaginate gastrulse are in several instances found coexisting in the same group renders it certain that there are not two independent phyla 'of the Metazoa, derived respectively from an invaginate and a delaminate gastrula 1 .

1 It is not difficult to picture a possible derivation of delamination from invagination ; while a comparison of the formation of the inner layers (mesoblast and hypoblast) in Ascetta (amongst the Sponges), and in the Echinodermata, shews a very simple way in which it is possible to conceive of a passage of delamination into invagination. In Ascetta the cells, which give rise to the mesoblast and hypoblast, are budded off from the inner wall of the blastosphere, especially at one point ; while in Echinodermata (fig. 199) there is a small invaginated sack which gives rise to the hypoblast, while from the walls of this sack amoeboid cells are budded off which give rise to a large part of the mesoblast. If we suppose the hypoblast cells budded off at one point in Ascetta gradually to form an invaginated sack, while the mesoblast cells continued to be budded off as before, we should pass from the delaminate type of tta t<> the invaginate type of an Echinoderm.


The four most important cases in which the two processes coexist are the Porifera, the Coelenterata, the Nemertea, and the Brachiopoda. In the cases of the Porifera and Ccelenterata, there do not appear to me to be any means of deciding which of these processes is derived from the other ; but in the Nemertea and the Brachiopoda the case is different. In all the types of Nemertea in which the development is relatively not abbreviated there is an invaginate gastrula, while in the types with a greatly abbreviated development there is a delaminate gastrula. It would seem to follow from this that a delaminate gastrula has here been a secondary result of an abbreviation in the development. In the Brachiopoda, again, the majority of types develop by a process of invagination, while Thecidium appears to develop by delamination ; here also the delaminate type would appear to be secondarily derived from the invaginate.

If these considerations are justified, delamination must be in some instances secondarily derived from invagination ; and this fact is so far an argument in favour of the more primitive nature of invagination ; though it by no means follows that in the invaginate process the steps by which the Metazoa were derived from the Protozoa are preserved.

It does not, therefore, seem possible to decide conclusively in favour of either of these processes by a comparison of the cases where they occur in the same groups.

The relative frequency of the two processes supplies us with another possible means for deciding between them ; and there is no doubt that here again the scale inclines towards invagination. It must, however, be borne in mind that the frequency of the process of invagination admits of another possible explanation. There is a continual tendency for the processes of development to be abbreviated and simplified, and it is quite possible that the frequent occurrence of invagination is due to the fact of its being, in most cases, the simplest means by which the twolayered condition can be reached. But this argument can have but little weight until it can be shewn in each case that invagination is a simpler process than delamination ; and it is rendered improbable by the cases already mentioned in which delamination has been secondarily derived from invagination.

If it were the case that the blastopore had ih all types the

22 2



same relation to the adult mouth, there would be strong grounds for regarding the invaginate gastrula as an ancestral form ; but the fact that this is by no means so is an argument of great weight in favour of some other explanation of the frequency of invagination.

The force of this consideration can best be displayed by a short summary of the fate of the blastopore in different forms.

The fate of the blastopore is so variable that it is difficult even to classify the cases which have been described.

(1) It becomes the permanent mouth in the following forms 1 : Ccelenterata. Pelagia, Cereanthus.

Turbellaria. Leptoplana (?), Thysanozoon.

Nemertea. Pilidium, larvae of the type of Desor.

Mollusca. In numerous examples of most Molluscan groups, except the


Chcetopoda. Most Oligochaeta, and probably many Polychseta. Gephyrea. Phascolosoma, Phoronis. Nematelminthes. Cucullanus.

(2) It closes in the position where the mouth is subsequently formed. Ccelenterata. Ctenophora (?).

Mollusca. In numerous examples of most Molluscan groups, except the

Cephalopoda. Crustacea. Cirripedia (?), some Cladocera (Moina) (?).

(3) It becomes the permanent anus. Mollusca. Paludina.

Chatopoda. Serpula and some other types. Echinodermata.Mmosl universally, except amongst the Crinoidea.

(4) It closes in the position where the anus is subsequently formed. Echinodermata. Crinoidea.

(5) It closes in a position which does not correspond or is not known to correspond 2 either with the future mouth or anus. Porifera Sycandra. Ccelenterata Chrysaora*, Aurelia*. Nemertea* Some larvae which develop without a metamorphosis. Rolifera*. Mollusca Cephalopoda. Polyzoa*. Brachiopoda Argiope, Terebratula, Terebratulina. Ch(Etopoda Euaxes. Discophora Clepsine. Gephyrea Bonellia*. Chatognatha. Crustacea Decapoda. Chordata.

The forms which have been classed together under the last heading vary considerably in the character of the blastopore. In some cases the fact of its not coinciding either with the mouth

1 The above list is somewhat tentative ; and future investigations will probably shew that many of the statements at present current about the position of the blastopore are inaccurate.

2 The forms in which the position of the blastopore in relation to the mouth or anus is not known <ire marked with an asterisk.


or anus appears to be due simply to the presence of a large amount of food-yolk. The cases of the Cephalopoda, of Euaxes, and perhaps of Clepsine and Bonellia, are to be explained in this way : in the case of all these forms, except Bonellia, the blastopore has the form of an elongated slit along the ventral surface. This type of blastopore is characteristic of the Mollusca generally, of the Polyzoa, of the Nematelminthes, and very possibly of the Chaetopoda and Discophora. In the Chaetognatha (fig. 209 B) the blastopore is situated, so far as can be determined, behind the future anus. In many Decapoda the blastopore is placed behind, but not far from, the anus. In the Chordata it is also placed posteriorly to the anus, and, remarkably enough, remains, in a large number of forms, for some time in connection with the neural tube by a neurenteric canal.

The great variations in the character of the gastrula, indicated in the above summary, go far to shew that if the gastrulae, as we find them in most types, have any ancestral characters, these characters can only be of the most general kind. This may best be shewn by the consideration of a few striking instances. The blastopore in Mollusca has an elongated slit-like form, extending along the ventral surface from the mouth to the anus. In Echinodermata it is a narrow pore, remaining as the anus. In most Chsetopoda it is a pore remaining as the mouth, but in some as the anus. In Chordata it is a posteriorlyplaced pore, opening into both the archenteron and the neural canal.

It is clearly out of the question to explain all these differences as having connection with the characters of ancestral forms. Many of them can only be accounted for as secondary adaptations for the convenience of development.

The epibolic gastrula of Mammalia (vide pp. 215 and 291) is a still more striking case of a secondary embryonic process, and is not directly derived from the gastrula of the lower Chordata. It probably originated in connection with the loss of food-yolk which took place on the establishment of a placental nutrition for the foetus. The epibolic gastrula of the Scorpion, of Isopods, and of other Arthropoda, seems also to be a derived gastrula. These instances of secondary gastrulse are very probably by no


means isolated, and should serve as a warning against laying too much stress upon the frequency of the occurrence of invagination. The great influence of the food-yolk upon the early development might be illustrated by numerous examples, especially amongst the Chordata (vide Chapter XL).

If the descendants of a form with a large amount of food-yolk in its ova were to produce ova with but little food-yolk, the type of formation of the germinal layers which would thereby result would be by no means the same as that of the ancestors of the forms with much food-yolk, but would probably be something very different, as in the case of Mammalia. Yet amongst the countless generations of ancestors of most existing forms, such oscillations in the amount of the food-yolk must have occurred in a large number of instances.

The whole of the above considerations point towards the view that the formation of the hypoblast by invagination, as it occurs in most forms at the present day, can have in many instances no special phylogenetic significance, and that the argument from frequency, in favour of invagination as opposed to delamination, is not of prime importance.

A third possible method of deciding between delamination and invagination is to be found in the consideration as to which of these processes occurs in the most primitive forms. If there were any agreement amongst primitive forms as to the type of their development this argument might have some weight. On the whole, delamination is, no doubt, characteristic of many primitive types, but the not infrequent occurrence of invagination in both the Ccelenterata and the Porifera the two groups which would on all hands be admitted to be amongst the most primitive deprives this argument of much of the value it might otherwise have.

To sum up considering the almost indisputable fact that both the processes above dealt with have in many instances had a purely secondary origin, no valid arguments can be produced to shew that either of them reproduces the mode of passage between the Protozoa and the ancestral two-layered Metazoa. These conclusions do not, however, throw any doubt upon the fact that the gastrula, however evolved, was a primitive form of the Metazoa ; since this conclusion is founded upon the actual



existence of adult gastrula forms independently of their occurrence in development.

Though embryology does not at present furnish us with a definite answer to the question how the Metazoa became developed from the Protozoa, it is nevertheless worth while reviewing some of the processes by which this can be conceived to have occurred.

On purely a priori grounds there is in my opinion more to be said for invagination than for any other view.

On this view we may suppose that the colony of Protozoa in the course of conversion into Metazoa had the form of a blastosphere ; and that at one pole of this a depression appeared. The cells lining this depression we



Fig. i, ovum; fig. 2, stage in segmentation; fig. 3, commencement of delamination after the appearance of a central cavity ; fig. 4, delamination completed, mouth forming at M. In figs, i, 2, and 3, EC, is ectoplasm, and En. is endoplasm. In fig. 4, EC. is epiblast, and En. hypoblast. E. and F. food particles.

may suppose to have been amoeboid, and to have carried on the work of digestion ; while the remaining cells were probably ciliated. The digestion may be supposed to have been at first carried on in the interior of the cells, as in the Protozoa; but, as the depression became deeper (in order to increase the area of nutritive cells and to retain the food) a digestive secretion probably became poured out from the cells lining it, and the mode of digestion generally characteristic of the Metazoa was thereby inaugurated. It may be noted that an intracellular protozoon type of digestion persists in the Porifera, and appears also to occur in many Ccelenterata, Turbellaria,


&c., though in most of these cases both kinds of digestion probably go on simultaneously 1 .

Another hypothetical mode of passage, which fits in with delamination, has been put forward by Lankester, and is illustrated by fig. 205. He supposes that at the blastosphere stage the fluid in the centre of the colony acquired special digestive properties ; the inner ends of the cells having at this stage somewhat different properties from the outer, and the food being still incepted by the surface of the cells (fig. 205, 3). In a later stage of the process the inner portions of the cells became separated off as the hypoblast ; while the food, though still ingested in the form of solid particles by the superficial cells, was carried through the protoplasm into the central digestive cavity. Later (fig. 205, 4), the point where the food entered became localised, and eventually a mouth became formed at this point.

The main objection which can be raised against Lankester's view is that it presupposes a type of delamination which does not occur in nature except in Geryonia.

Metschnikoff has propounded a third view with reference to delamination. He starts as before with a ciliated blastosphere. He next supposes the cells from the walls of this to become budded off into the central cavity, as in Eucope (fig. 202), and to lose their cilia. These cells give rise to an internal parenchyma, which carries on an intracellular digestion. At a later stage a central digestive cavity is supposed to be formed. This view of the passage from the protozoon to the metazoon state, though to my mind improbable in itself, fits in very well with the ontogeny of the lower Hydrozoa.

Another view has been put forward by myself in the chapter on the Porifera*, to the effect that the amphiblastula larva of Calcispongias may be a transitional form between the Protozoa and the Metazoa, composed of a hemisphere of nutritive amoeboid cells, and a hemisphere of ciliated cells. The absence of such a larval form in the Ccelenterata and higher Metazoa is opposed, however, to this larva being regarded as a transitional form, except for the Porifera.

It is obvious that so long as there is complete uncertainty as to the value to be attached to the early developmental processes, it is not possible to decide from these processes whether there is only a single metazoon phylum or whether there may not be two or more such phyla. At the same time there appear to be strong

1 J. Parker, "On the Histology of Hydra fusca," Quart. Journ. Micr. Science, vol. xx. 1880; and El. Metschnikoff, " Ueb. die intracellulare Verdauung bei Ccelenteraten," Zoologischer Anzeiger, No. 56, vol. in. 1880 and Lankester, " On the intracellular digestion and endoderm of Limnocodium, " Quart. Journ. Micr. Science, vol. xxi. 1881.

! Vol. n. p. 149.


arguments for regarding the Porifera as a phylum of the Metazoa derived independently from the Protozoa. This seems to me to be shewn (i) by the striking larval peculiarities of the Porifera ; (2) by the early development of the mesoblast in the Porifera, which stands in strong contrast to the absence of this layer in the embryos of most Ccelenterata ; and above all, (3) by the remarkable characters of the system of digestive channels. A further argument in the same direction is supplied by the fact that the germinal layers of the Sponges very probably do not correspond physiologically to the germinal layers of other types. The embryological evidence is insufficient to decide whether the amphiblastula larva is, as suggested above, to be regarded as the larval ancestor of the Porifera.

Homologies of the germinal layers. The question as to how far there is a complete homology between the two primary germinal layers throughout the Metazoa was the third of the questions proposed to be discussed here.

Since there are some Metazoa with only two germinal layers, and other Metazoa with three, and since, as is shewn in the following section, the third layer or mesoblast can only be regarded as a derivative of one or both the primary layers, it is clear that a complete homology between the two primary germinal layers does not exist.

That there is a general homology appears on the other hand hardly open to doubt.

The primary layers are usually continuous with each other, near one or both (when both are present) the openings of the alimentary tract.

As a rule an oral and anal section of the alimentary tract the stomodaeum and proctodaeum are derived from the epiblast ; but the limits of both these sections are so variable, sometimes even in closely allied forms, that it is difficult to avoid the conclusion that there is a border-land between the epiblast and hypoblast, which appears by its development to belong in some forms to the epiblast and in other forms to the hypoblast. If this is not the case it is necessary to admit that there are instances in which a very large portion of the alimentary canal is phylogenetically an epiblastic structure. In some of the Isopods, for example, the stomodaeum and proctodaeum give


rise to almost the whole of the alimentary canal with its appendages, except the liver.

The origin of the Mesoblast. A diploblastic condition of the organism preceded, as we have seen, the triploblastic. The epiblast during the diploblastic condition was, as appears from such forms as Hydra, especially the sensory and protective layer, while the hypoblast was the secretory and assimilating layer; both layers giving rise to muscular elements. It must not, however, be supposed that in the early diploblastic ancestors there was a complete differentiation of function, but there is reason to think that both the primary layers retained an indefinite capacity for developing into any form of tissue 1 . The fact of the triploblastic condition being later than the diploblastic proves in a conclusive way that the mesoblast is a derivative of one or both the primary layers. In the Ccelenterata we can study the actual origin from the two primary layers of various forms of tissue which in the higher types are derived from the mesoblast 2 . This fact, as well as general a priori considerations, conclusively prove that the mesoblast did not at first originate as a mass of independent cells between the two primary layers, but that in the first instance it gradually arose as differentiations of the two layers, and that its condition in the embryo as an independent layer of undifferentiated cells is a secondary condition, brought about by the general tendency

1 The Hertwigs (No. 270) have for instance shewn that nervous structures are developed in the hypoblast in the Actinozoa and other Coelenterata.

2 There is considerable confusion in the use of the names for the embryonic layers. In some cases various tissues formed by differentiations of the primary layers have been called mesoblast. Schultze, and more recently the Hertwigs, have pointed out the inconvenience of this nomenclature. In the case of the Coelenterata it is difficult to decide in certain instances (e.g. Sympodium) whether the cells which give rise to a particular tissue of the adult are to be regarded as forming a mesoblast, i.e. a middle undifferentiated layer of cells, or whether they arise as already histologically differentiated elements from one of the primary layers. The attempt to distinguish by a special nomenclature the epiblast and hypoblast after and before the separation of the mesoblast, which has been made by Allen Thomson (No. 1), appears incapable of being consistently applied, though it is convenient to distinguish a primary and a secondary hypoblast. A proposal of the Hertwigs to adopt special names for the outer and inner limiting membranes of the adult, and for the interposed mass of organs, appears to me unnecessary.


towards a simplification of development, and a retardation of histological differentiation 1 .

The Hertwigs have recently attempted (No. 271) to distinguish two types of differentiation of the mesoblast, viz. (i) a direct differentiation from the primitive epithelial cells ; (2) a differentiation from primitively indifferent cells budded off into the gelatinous matter between the two primary layers.

It is quite possible that this distinction may be well founded, but no conclusive evidence of the occurrence of the second process has yet been adduced. The Ctenophora are the type upon which special stress is laid, but the early passage of amoeboid cells into the gelatinous tissue, which subsequently become muscular, is very probably an embryonic abbreviation ; and it is quite possible that these cells may phylogenetically have originated from epithelial cells provided with contractile processes passing through the gelatinous tissue.

The conversion of non-embryonic connective-tissue cells into muscle cells in the higher types has been described, but very much more evidence is required before it can be accepted as a common occurrence.

In addition to the probably degraded Dicyemida:: and Orthonectidae, the Ccelenterata are the only group in which a true mesoblast is not always present. In other words, the Ccelenterata are the only group in which there is not found in the embryo an undifferentiated group of cells from which the majority of the organs situated between the epidermis and the alimentary epithelium are developed.

The organs invariably derived, in the triploblastic forms, from the mesoblast, are the vascular and lymphatic systems, the muscular system, and the greater part of the connective tissue and the excretory and generative (?) systems. On the other hand, the nervous systems (with a few possible exceptions) and organs of sense, the epithelium of most glands, and a few exceptional connective-tissue organs, as for example the notochord, are developed from the two primary layers.

The fact of the first-named set of organs being invariably derived from the mesoblast points to the establishment of the two following propositions: (i) That with the differenti 1 The causes which give rise to a retardation of histological differentiation will be dealt with in the second part of this chapter which deals with larval characters and larval forms.


ation of the mesoblast as a distinct layer by the process already explained, the two primary layers lost for the most part the capacity they primitively possessed of giving rise to muscular and connective-tissue differentiations 1 , to the epithelium of the excretory organs, and to generative cells. (2) That the mesoblast throughout the triploblastic Metazoa, in so far as these forms have sprung from a common triploblastic ancestor, is an homologous structure.

The second proposition follows from the first. The mesoblast can only have ceased to be homologous throughout the triploblastica by additions from the two primary layers, and the existence of such additions is negatived by the first proposition.

These two propositions, which hang together, are possibly only approximately true, since it is quite possible that future investigations may shew that differentiations of the two primary layers are not so rare as has been hitherto imagined.

Ranvier 2 finds that the muscles of the sweat-glands are developed from the inner part of the layer of epiblast cells, invaginated to form these glands.

Gotte 3 describes the epiblast cells of the larva of Comatula as being at a certain stage contractile and compares them with the epithelio-muscular cells of Hydra. These cells would appear subsequently to be converted into a simple cuticular structure.

It is moreover quite possible that fresh differentiations from the two primary layers may have arisen after the triploblastic condition had been established, and by the process of simplification of development and precocious segregation, as Lankester calls it, have become indistinguishable from the normal mesoblast. In spite of these exceptions it is probable that the major part of the muscular system of all existing triploblastic forms has been differentiated from the muscular system of the ancestor or ancestors (if there is more than one phylum) of the triplo 1 The connective-tissue test of the Tunicata, though derived from the epiblast, is not really an example of such a differentiation.

1 M. L. Ranvier. " Sur la stricture des glandes sudoripares." Comptes Rendus, Dec. 29, 1879.

1 A. Gotte, "Vergleich. Entwick. d. Comatula mediterranea." Archiv f. mikr. Anat. vol. XI I. p. 597.



blastica. In the case of other tissues there are a few instances which might be regarded as examples of an organ primitively developed in one of the two primary layers having become secondarily carried into the mesoblast. The notochord has sometimes been cited as such an organ, but, as indicated in a previous chapter, it is probable that its hypoblastic origin can always be demonstrated.



A. Stage when the four hypoblast cells are nearly enclosed.

B. Stage after the formation of the mesoblast has commenced by an infolding of the lips of the blastopore.

ep. epiblast; me. mesoblast; bl. blastopore.

The nervous system, although imbedded in mesoblastic derivates in the adults of all the higher triploblastica, retains with marvellous constancy its epiblastic origin (though it is usually separated from the epiblast prior to its histogenic differentiation) ; yet in the Cephalopoda, and some other Mollusca, the evidence is in favour of its developing in the mesoblast. Should future investigations confirm these conclusions, a good example will be afforded of an organ changing the layer from which it usually develops 1 . The explanation of such a change would be precisely the same as that already given for the mesoblast as a whole.

The actual mode of origin of various tissues, which in the true triploblastic forms arise in mesoblast, can be traced in the

1 The Hertvvigs hold that there is a distinct part of the nervous system which was at first differentiated in the mesoblast in many types, amongst others the Mollusca. The evidence in favour of this view is extremely scanty and the view itself appears to me highly improbable.


Ccelenterata 1 . In this group the epiblast and hypoblast both give rise to muscular and connective-tissue elements ; and although the main part of the nervous system is formed in the epiblast, it seems certain that in some types nerves may be derived from the hypoblast' 2 . These facts are extremely interest


PICEUS. (After Kowalevsky.)

A. Section through an embryo at the point where the two germinal folds most approximate.

B. Section through an embryo, in the anterior region where the folds of the amnion have not united.

gg. germinal groove; me. mesoblast; am. amnion; yk. yolk.

ing, but it is by no means certain that any conclusions can be directly drawn from them as to the actual origin of the mesoblast in the triploblastic forms, till we know from what diploblastic forms the triploblastica originated. All that they shew is that any of the constituents of the mesoblast may have originated from either of the primitive layers.

1 The reader is referred for this subject to the valuable memoirs which have been recently published by the Hertwigs, especially to No. 270. He will find a general account of the subject written before the appearance of the Hertwigs' memoir in pp. 180-182 of Volume II. of this treatise.

- It would be interesting to know the history of the various nervous structures found in the walls of the alimentary tract in the higher forms. I have shewn (Development of Elasmobranch Fishes, p. 172) that the central part of the sympathetic system is derived from the epiblast. It would however be well to work over the development of Auerbach's plexus.



For further light as to the origin of the mesoblast, it is necessary to turn to its actual development.

The following summary illustrates the more important modes in which the mesoblast originates. B


A. Section through part of the ovum during segmentation, n. nuclei ; w.y. white yolk ; y.p. yolk pyramids ; c. central yolk mass.

B. and C. Longitudinal sections of the gastrula stage, a. archenteron ; b. blastopore; ms. mesoblast; ec. epiblast; en. hypoblast, distinguished from epiblast by shading.

D. Highly magnified view of anterior lip of blastopore, to shew the origin of the primary mesoblast from the wall of the archenteron. /. ms. primary mesoblast ; ec. epiblast ; en. hypoblast.

E. Two hypoblast cells to shew the amoeba-like absorption of yolk spheres. y. yolk ; n. nucleus ; p. pseudopodial process.

F. Hypoblast cells giving rise endogenously to the secondary mesoblast (s.tns.) ; n. nucleus.

I. It grows inwards from the lips of the blastopore as a pair of bands. In these cases it may originate (a) from cells which are clearly hypoblastic, (b} from cells which are clearly epiblastic, (c) from cells which cannot be regarded as belonging to either layer.

Mollusca. Gasteropoda, Cephalopoda, and Lamellibranchiata. In Gasteropoda and Lamellibranchiata the mesoblast sometimes originates



from a pair of cells at the lips of the blastopore, though very probably some of the elements subsequently come from the epiblast ; and in Cephalopoda it begins as a ring of cells round the edge of the blastoderm.

Polyzoa Entoprocta. It originates from a pair of cells at the lips of the blastopore.

Chaetopoda. Euaxes. It arises as a ridge of cells at the lips of the blastopore (fig. 200).

Gephyrea. Bonellia. It arises (fig. 206) as an infolding of the epiblastic lips of the blastopore.

Nematelminthes. Cucullanus. It grows backwards from the hypoblast cells at the persistent oral opening of the blastopore.

Tracheata. Insecta. It grows inwards from the lips of the germinal groove (fig. 207), which probably represent the remains of a blastopore. Part of the mesoblast is probably also derived from the yolk-cells. A similar though more modified development of the mesoblast occurs in the Araneina (fig. 214).

Crustacea. Decapoda. It partly grows in from the hypoblastic lips of the blastopore, and is partly derived from the yolk-cells (fig. 208).


after Biitschli, and B. after Kowalevsky.) The three embryos are represented in the same positions.

A. Represents the gastrula stage.

B. Represents a succeeding stage, in which the primitive archenteron is commencing to be divided into three.

C. Represents a later stage, in which the mouth involution (m) has become continuous with the alimentary tract, and the blastopore has become closed.

m. mouth; al. alimentary canal; ae. archenteron; bl.p. blastopore; pv. perivisceral cavity; sp. splanchnic mesoblast; so. somatic mesoblast; ge. generative organs.

2. The mesoblast is developed from the walls of hollow outgrowths of the archenteron, the cavities of which become the body cavity.



Brachiopoda. The walls of a pair of outgrowths form the whole of the mesoblast.

Chaetognatha. The mesoblast arises in the same manner as in the Brachiopoda (fig. 209).

Echinodermata. The lining of the peritoneal cavity is developed from the walls of outgrowths of the archenteron, but the greater part of the mesoblast is derived from the amoeboid cells budded off from the walls of the archenteron (fig. 210).


Mp. Pld.


Vpv. vaso-peritoneal vesicle; ME. mesenteron; Sip., Ptd. blastopore, proctodjeum.

Enteropneusta (Balanoglossus). The body cavity is derived from two pairs of alimentary diverticula, the walls of which give rise to the greater part of the mesoblast.

Chordata. Paired archenteric outgrowths give rise to the whole mesoblast in Amphioxus (fig. 211), and the mode of formation of the mesoblast in other Chordata is probably secondarily derived from this.

3. The cells which will form the mesoblast become marked out very early, and cannot be regarded as definitely springing from either of the primary layers.

Turbellaria. Leptoplana (fig. 212), Planaria polychroa (?).

Chsetopoda. Lumbricus, &c.


It is very possible that the cases quoted under this head ought more properly to belong to group i.

4. The mesoblast cells are split off from the epiblast.

Nemertea. Larva of Desor. The mesoblast is stated to be split off from the four invaginated discs.

B. III. 23



5. The mcsoblast is split off from the hypoblast.

Nemertea. Some of the types without a metamorphosis.

Mollusca. Scaphopoda. It is derived from the lateral and ventral cells of the hypoblast.

Oephyrea. Phascolosoma.

Vertebrata. In most of the Ichthyopsida the mesoblast is derived from the hypoblast (fig. 213). In some types (i.e. most of the Amniota) the mesoblast might be described as originating at the lips of the blastopore (primitive streak).

6. The mesoblast is derived from both germinal layers.

Tracheata. Araneina (fig. 214). It is derived partly from cells split off from the epiblast and partly from the yolk-cells ; but it is probable that the statement that the mesoblast is derived from both the germinal layers is only formally accurate ; and that the derivation of part of the mesoblast from the yolk-cells is not to be interpreted as a derivation from the hypoblast.

Amniota. The derivation of the mesoblast of the Amniota from both the primary germinal layers is without doubt a secondary process.

The conclusions to be drawn from the above summary are by no means such as might have been anticipated. The analogy of the Ccelenterata would lead us to expect that the mesoblast

FIG. 211.

A. B.


(After Kowalevsky.) Section at gastrula stage. Section of a somewhat older embryo. C. Section through the anterior part of still older embryo. np. neural plate; nc. neural canal; mcs. archenteron in A, and mesenteron in B and C ; ch. notochord ; so. mesoblastic somite.

would be derived partly from the epiblast and partly from the hypoblast. Such, however, is not for the most part the case, though more complete investigations may shew that there are a greater number of instances in which the mesoblast has a mixed origin than might be supposed from the above summary.


I have attempted to reduce the types of development of the mesoblast to six ; but owing to the nature of the case it is not always easy to distinguish the first of these from the last fourOf the six types the second will on most hands be admitted to be the most remarkable. The formation of hollow outgrowths of the archenteron, the cavities of which give rise to the body cavity, can only be explained on the supposition that the body cavity of the types in which such outgrowths occur is derived from diverticula cut off from the alimentary tract. The lining epithelium of the diverticula the peritoneal epithelium is clearly part of the primitive hypoblast, and this part of the mesoblast is clearly hypoblastic in origin.


THREE STAGES OF DEVELOPMENT. (After Hallez.) cp. epiblast ; ;;/. mesoblast; hy. yolk-cells (hypoblast); bl. blastopore.

In the case of the Chaetognatha (Sagitta), Brachiopoda, and Amphioxus, the whole of the mesoblast originates from the walls of the diverticula ; while in the Echinodermata the walls of the diverticula only give rise to the vaso-peritoneal epithelium, the remainder of the mesoblast being derived from amoeboid cells which spring from the walls of the archenteron before the origin of the vaso-peritoneal outgrowths (figs. 199 and 210).

Reserving for the moment the question as to what conclusions can be deduced from the above facts as to the origin of the mesoblast, it is important to determine how far the facts of embryology warrant us in supposing that in the whole of the triploblastic forms the body cavity originated from the alimentary diverticula. There can be but little doubt that the mode of origin of the mesoblast in many Vertebrata, as two solid plates split off from the hypoblast, in which a cavity is secondarily developed, is an abbreviation of the process observable in Amphioxus ; but this process approaches in some forms of




Vertebrata to the ingrowth of the mesoblast from the lips of the blastopore.

It is, therefore, highly _ en A.

probable that the paired ingrowths of the mesoblast from the lips of the blastopore may have been in the first instance derived from a pair of archenteric diverticula. This process of formation of the mesoblast is, as may be seen by reference to the summary, the most frequent, including as it does the Chaetopoda,




While there is no difficulty in the view that the body cavity may have originated from a pair of enteric diverticula in the case of the forms where a body cavity is present, there is a considerable difficulty in holding this view, for forms in which there is no body cavity distinct from the alimentary diverticula.

Of these types the Platyelminthes are the most striking. It is, no doubt, possible that a body cavity may have existed in the Platyelminthes, and become lost ; and the case of the Discophora, which in their muscular and connective tissue systems as well as in the absence of a body cavity resemble the Platyelminthes, may be cited in favour of this view, in that, being closely related to the Chaetopoda, they are almost certainly descended from ancestors with a true body cavity. The usual view of the primitive character of the

nig. medullary groove ; ep. epiblast ; ;;/. mesoblast ; hy. hypoblast ; cells formed around the nuclei of the yolk which have entered the hypoblast.

1 The wide occurrence of this process was first pointed out by Rabl. He holds, however, a peculiar modification of the gastrsea theory, for which I must refer the reader to his paper (No. 284) ; according to this theory the mesoblast has sprung from a zone of cells of the blastosphere, at the junction between the cells which will be invaginated and the epiblast cells. In the bilateral blastosphere, from which he holds that all the higher forms (Bilateralia) have originated, these cells had a bilateral arrangement, and thus the bilateral origin of the mesoblast is explained. The origin of the mesoblast from the lips of the blastopore is explained by the position of its mother-cells in the blastosphere. It need scarcely be said that the views already put forward as to the probable mode of origin of the mesoblast, founded on the analogy of the Ccelenterata, are quite incompatible with Rabl's theories.


Platyelminthes, which has much to support it, is, however, opposed to the idea that the body cavity has disappeared.

If Kowalevsky 1 is right in stating that he has found a form intermediate between the Ccelenterata and the Platyelminthes, there will be strong grounds for holding that the Platyelminthes are, like the Ccelenterata, forms the ancestors of which were not provided with a body cavity.

Perhaps the triploblastica are composed of two groups, viz. (i) a more ancestral group (the Platyelminthes), in which there is no body cavity as dis

FIG. 214. SECTION THROUGH AN EMBRYO OK AGEI.ENA LABYRINTHICA. The section is represented with the ventral plate upwards. In the ventral plate is seen a keel-like thickening, which gives rise to the main mass of the mesoblast. yk. yolk divided into large polygonal cells, in several of which are nuclei.

tinct from the alimentary, and (2) a group descended from these, in which two of the alimentary diverticula have become separated from the alimentary tract to form a body cavity (remaining triploblastica). However this may be, the above considerations are sufficient to shew how much there is that is still obscure with reference even to the body cavity.

If embryology gives no certain sound as to the questions just raised with reference to the body cavity, still less is it to be hoped that the remaining questions with reference to the origin of the mesoblast can be satisfactorily answered. It is clear, in the first place, from an inspection of the summary given above, that the process of development of the mesoblast is, in all the higher forms, very much abbreviated and modified. Not only is its differentiation relatively deferred, but it does not in most cases originate, as it must have done to start with, as a more or

1 Zoologischer Anzeiger, No. 52, p. 140. This form has been named by Kowalevsky Cceloplana Metschnikowii. Kowalevsky's description appears, however, to be quite compatible with the view that this form is a creeping Ctenophor, in no way related to the Turbellarians.


less continuous sheet, split off from parts of one or both the primary layers. It originates in most cases from the hypoblast, and although the considerations already urged preclude us from laying very great stress on this mode of origin, yet the derivation of the mesoblast from the walls of archenteric outgrowths suggests the view that the whole, or at any rate the greater part, of the mesoblast primitively arose by a process of histogenic differentiation from the walls of the archenteron or rather from diverticula of these walls. This view, which was originally put forward by myself (No. 260), appears at first sight very improbable, but if the statement of the Hertwigs (No. 270), that there is a large development of a hypoblastic muscular system in the Actinozoa, is well founded, it cannot be rejected as impossible. Lankester (No. 279), on the other hand, has urged that the mode of origin of the mesoblast in the Echinodermata is more primitive ; and that the amoeboid cells which here give rise to the muscular and connective tissues represent cells which originally arose from the whole inner surface of the epiblast. It is, however, to be noted that even in the Echinodermata the amoeboid cells actually arise from the hypoblast, and their mode of origin may, therefore, be used to support the view that the main part of the muscular system of higher types is derived from the primitive hypoblast.

The great changes which have taken place in the development of the mesoblast would be more intelligible on this view than on the view that the major part of the mesoblast primitively originated from the epiblast. The presence of food-yolk is much more frequent in the hypoblast than in the epiblast ; and it is well known that a large number of the changes in early development are caused by food-yolk. If, therefore, the mesoblast has been derived from the hypoblast, many more changes might be expected to have been introduced into its early development than if it had been derived from the epiblast. At the same time the hypoblastic origin of the mesoblast would assist in explaining how it has come about that the development of the nervous system is almost always much less modified than that of the mesoblast, and that the nervous system is not, as might, on the grounds of analogy, have been anticipated, as a rule secondarily developed in the mesoblast.


The Hertwigs have recently suggested in their very interesting memoir (No. 271) that the Triploblastica are to be divided into two phyla, (i) the Enteroccela, and (2) the Pseudocoela ; the former group containing the Chaetopoda, Gephyrea, Brachiopoda, Nematoda, Arthropoda, Echinodermata, Enteropneusta and Chordata ; and the latter the Mollusca, Polyzoa, the Rotifera, and Platyelminthes.

The Enteroccela are forms in which the primitive alimentary diverticula have given origin to the body cavity, while the major part of the muscular system has originated from the epithelial walls of these diverticula, part however being in many cases also derived from the amoeboid cells, called by them mesenchyme, by the second process of mesoblastic differentiation mentioned on p. 347.

In the Pseudoccela the muscular system has become differentiated from mesenchyme cells ; while the body cavity, where it exists, is merely a split in the mesenchyme.

It is impossible for me to attempt in this place to state fully, or do justice to, the original and suggestive views contained in this paper. The general conclusion I cannot however accept. The views of the Hertwigs depend to a large extent upon the supposition that it is possible to distinguish histologically muscle cells derived from epithelial cells, from those derived from mesenchyme cells. That in many cases, and strikingly so in the Chordata, the muscle cells retain clear indications of their primitive origin from epithelial cells, I freely admit ; but I do not believe either that its histological character can ever be conclusive as to the non-epithelial origin of a muscle cell, or that its derivation in the embryo from an indifferent amoeboid cell is any proof that it did not, to start with, originate from an epithelial cell.

I hold, as is clear from the preceding statements, that such immense secondary modifications have taken place in the development of the mesoblast, that no such definite conclusions can be deduced from its mode of development as the Hertwigs suppose.

In support of the view that the early character of embryonic cells is no safe index as to their phylogenetic origin, I would point to the few following facts.

(1) In the Porifera and many of the Ccelenterata (Eucope polystyla, Geryonia, &c.) the hypoblast (endoderm) originates from cells, which according to the Hertwigs' views ought to be classed as mesenchyme.

(2) In numerous instances muscles which have, phylogenetically, an undoubted epithelial origin, are ontogenetically derived from cells which ought to be classed as mesenchyme. The muscles of the head in all the higher Vertebrata, in which the head cavities have disappeared, are examples of this kind ; the muscles of many of the Tracheata, notably the Araneina, must also be placed in the same category.

(3) The Mollusca are considered by the Hertwigs to be typical Pseudocoela. A critical examination of the early development of the mesoblast in these forms demonstrates however that with reference to the mesoblast they


must be classed in the same group as the Cluetopoda. The mesoblast (Vol. II. p. 227) clearly originates as two bands of cells which grow inwards from the blastopore, and in some forms (Paludina, Vol. II. fig. 107) become divided into a splanchnic and somatic layer, with a body cavity between them. All these processes are such as are, in other instances, admitted to indicate Enteroccclous affinities.

The subsequent conversion of the mesoblast elements into amoeboid cells, out of which branched muscles are formed, is in my opinion simply due to the envelopment of the soft Molluscan body within a hard shell.

In addition to these instances I may point out that the distinction between the Pseudocoela and Enteroccela utterly breaks down in the case of the Discophora, and the Hertwigs have made no serious attempt to discuss the characters of this group in the light of their theory, and that the derivation of the Echinoderm muscles from mesenchyme cells is a difficulty which is very slightly treated.


Preliminary considerations. In a general way two types of development may be distinguished, viz. a foetal type and a larval type. In the foetal type animals undergo the whole or nearly the whole of their development within the egg or within the body of the parent, and are hatched in a condition closely resembling the adult ; and in the larval type they are born at an earlier stage of development, in a condition differing to a greater or less extent from the adult, and reach the adult state either by a series of small steps, or by a more or less considerable metamorphosis.

The satisfactory application of embryological data to morphology depends upon a knowledge of the extent to which the record of ancestral history has been preserved in development. Unless secondary changes intervened this record would be complete ; it becomes therefore of the first importance to the cmbryologist to study the nature and extent of the secondary changes likely to occur in the fcetal or the larval state.

The principles which govern the perpetuation of variations which occur in either the larval or the fcetal state are the same as those for the adult condition. Variations favourable to the survival of the species are equally likely to be perpetuated, at whatever period of life they occur, prior to the loss of the reproductive powers. The possible nature and extent of the


secondary changes which may have occurred in the developmental history of forms, which have either a long larval existence, or which are born in a nearly complete condition, is primarily determined by the nature of the favourable variations which can occur in each case.

Where the development is a fcetal one, the favourable variations which can most easily occur are (i) abbreviations, (2) an increase in the amount of food-yolk stored up for the use of the developing embryo. Abbreviations take place because direct development is always simpler, and therefore more advantageous; and, owing to the fact of the foetus not being required to lead an independent existence till birth, and of its being in the meantime nourished by food-yolk, or directly by the parent, there are no physiological causes to prevent the characters of any stage of the development, which are of functional importance during a free but not during a fcetal existence, from, disappearing from the developmental history. All organs of locomotion and nutrition not required by the adult will, for this reason, obviously have a tendency to disappear or to be reduced in foetal developments; and a little consideration will shew that the ancestral stages in the development of the nervous and muscular systems, organs of sense, and digestive system will be liable to drop out or be modified, when a simplification can thereby be effected. The circulatory and excretory systems will not be modified to the same extent, because both of them are usually functional during fcetal life.

The mechanical effects of food-yolk are very considerable, and numerous instances of its influence will be found in the earlier chapters of this work 1 . It mainly affects the early stages of development, i.e. the form of the gastrula, &c.

The favourable variations which may occur in the free larva are much less limited than those which can occur in the fcetus. Secondary characters are therefore very numerous in larvae, and there may even be larvae with secondary characters only, as, for instance, the larvae of Insects.

In spite of the liability of larvae to acquire secondary characters, there is a powerful counterbalancing influence tending

1 For numerous instances of this kind, vide Chapter XI. of Vol. in.


towards the preservation of ancestral characters, in that larvae are necessarily compelled at all stages of their growth to retain in a functional state such systems of organs, at any rate, as are essential for a free and independent existence. It thus comes about that, in spite of the many causes tending to produce secondary changes in larvae, there is always a better chance of larvae repeating, in an unabbreviated form, their ancestral history, than is the case with embryos, which undergo their development within the egg.

It may be further noted as a fact which favours the relative retention by larvae of ancestral characters, that a secondary larval stage is less likely to be repeated in development than an ancestral stage, because there is always a strong tendency for the former, which is a secondarily intercalated link in the chain of development, to drop out by the occurrence of a reversion to the original type of development.

The relative chances of the ancestral history being preserved in the foetus or the larva may be summed up in the following way : There is a greater chance of the ancestral history being lost in forms which develop in the egg ; and of its being masked in those which are hatched as larvae.

The evidence from existing forms undoubtedly confirms the a priori considerations just urged 1 . This is well shewn by a study of the development of Echinodermata, Nemertea, Mollusca, Crustacea, and Tunicata. The free larvae of the four first groups are more similar amongst themselves than the embryos which develop directly, and since this similarity cannot be supposed to be due to the larvae having been modified by living under precisely similar conditions, it must be due to their retaining common ancestral characters. In the case of the Tunicata the free larvae retain much more completely than the embryos certain characters such as the notochord, the cerebrospinal canal, etc., which are known to be ancestral.

1 It has long been known that land and freshwater forms develop without a metamorphosis much more frequently than marine forms. This is probably to be explained by the fact that there is not the same possibility of a land or freshwater species extending itself over a wide area by the agency of free larvre, and there k, therefore, much less advantage in the existence of such larva:; while the fact of such larviu being more liable to be preyed upon than eggs, which are either concealed, or carried about by the parent, might render a larval stage absolutely disadvantageous.


Types of Larvae. Although there is no reason to suppose that all larval forms are ancestral, yet it seems reasonable to anticipate that a certain number of the known types of larvae would retain the characters of the ancestors of the more important phyla of the animal kingdom.

Before examining in detail the claims of various larvae to such a character, it is necessary to consider somewhat more at length the kind of variations which are most likely to occur in larval forms.

It is probable a priori that there are two kinds of larvae, which may be distinguished as primary and secondary larvae. Primary larvae are more or less modified ancestral forms, which have continued uninterruptedly to develop as free larvae from the time when they constituted the adult form of the species. Secondary larvae are those which have become introduced into the ontogeny of species, the young of which were originally hatched with all the characters of the adult; such secondary larvae may have originated from a diminution of food-yolk in the egg and a consequently earlier commencement of a free existence, or from a simple adaptive modification in the just hatched young. Secondary larval forms may resemble the primary larval forms in cases where the ancestral characters were retained by the embryo in its development within the egg; but in other instances their characters are probably entirely adaptive.

Causes tending to produce secondary changes in larv<z. The modes of action of natural selection on larvae may probably be divided more or less artificially into two classes.

1. The changes in development directly produced by the existence of a larval stage.

2. The adaptive changes in a larva acquired in the ordinary course of the struggle for existence.

The changes which come under the first head consist essentially in a displacement in the order of development of certain organs. There is always a tendency in development to throw back the differentiation of the embryonic cells into definite tissues to as late a date as possible. This takes place in order to enable the changes of form, which every organ undergoes, in repeating even in an abbreviated way its phylogenetic history, to be effected with the least expenditure of energy. Owing to


this tendency it comes about that when an organism is hatched as a larva many of the organs are still in an undifferentiated state, although the ancestral form which this larva represents had all its organs fully differentiated. In order, however, that the larva may be enabled to exist as an independent organism, certain sets of organs, e.g. the muscular, nervous, and digestive systems, have to be histologically differentiated. If the period of foetal life is shortened, an earlier differentiation of certain organs is a necessary consequence ; and in almost all cases the existence of a larval stage causes a displacement in order of development of organs, the complete differentiation of many organs being retarded relatively to the muscular, nervous, and digestive systems.

The possible changes under the second head appear to be unlimited. There is, so far as I see, no possible reason why an indefinite number of organs should not be developed in larvae to protect them from their enemies, and to enable them to compete with larvae of other species, and so on. The only limit to such development appears to be the shortness of larval life, which is not likely to be prolonged, since, ceteris paribus, the more quickly maturity is reached the better it is for the species.

A very superficial examination of marine larvae shews that there are certain peculiarities common to most of them, and it is important to determine how far such peculiarities are to be regarded as adaptive. Almost all marine larvae are provided with well-developed organs of locomotion, and transparent bodies. These two features are precisely those which it is most essential for such larvae to have. Organs of locomotion are important, in order that larvae may be scattered as widely as possible, and so disseminate the species ; and transparency is very important in rendering larvae invisible, and so less liable to be preyed upon by their numerous enemies 1 .

These considerations, coupled with the fact that almost all free-swimming animals, which have not other special means of protection, are transparent, seem to shew that the transparency

1 The phosphorescence of many larvze is very peculiar. I should have anticipated that phosphorescence would have rendered them much more liable to be captured by the forms which feed upon them; and it is difficult to see of what advantage it can be to them.


of larvae at all events is adaptive ; and it is probable that organs of locomotion are in many cases specially developed, and not ancestral.

Various spinous processes on the larvae of Crustacea and Teleostei are also examples of secondarily acquired protective organs.

These general considerations are sufficient to form a basis for the discussion of the characters of the known types of larvae.

The following table contains a list of the more important of such larval forms :

DICYEMID^. The Infusoriform larva (vol. n. fig. 62).

PORIFERA. (a) The Amphiblastula larva (fig. 215), with one-half of the body ciliated, and the other half without cilia; (b) an oval uniformly ciliated larva, which may be either solid or have the form of a vesicle.

CCELENTERATA. The planula (fig. 216).

TURBELLARIA. (a) The eight-lobed larva of Miiller (fig. 222); (b) the larvae of Gotte and Metschnikoff, with some Pilidium characters.

NEMERTEA. The Pilidium (fig. 221).

TREMATODA. The Cercaria.

ROTIFERA. The Trochosphere-like larvae of Brachionus (fig. 217) and Lacinularia.

MOLLUSCA. The Trochosphere larva (fig. 218), and the subsequent Veliger larva (fig. 219).

BRACHIOPODA. The three-lobed larva, with a postoral ring of cilia (fig. 220).

POLYZOA. A larval form with a single ciliated ring surrounding the mouth, and an aboral ciliated ring or disc (fig. 228).

CH/ETOPODA. Various larval forms with many characters like those of the molluscan Trochosphere, frequently with distinct transverse bands of cilia. They are classified as Atrochoe, Mesotrochse, Telotrochse (fig. 225 A and fig. 226), Polytrochae, and Monotrochae (fig. 225 B).

GEPHYREA NUDA. Larval forms like those of preceding groups. A specially characteristic larva is that of Echiurus (fig. 227).

GEPHYREA TUBICOLA. Actinotrocha (fig. 230), with a postoral ciliated ring of arms.

MYRIAPODA. A functionally hexapodous larval form is common to all the Chilognatha (vol. n. fig. 174).

INSECTA. Various secondary larval forms.

CRUSTACEA. The Nauplius (vol. n. fig. 208) and the Zosea (vol. II. fig. 210).

ECHINODERMATA. The Auricularia (fig. 223 A), the Bipinnaria (fig. 223 B), and the Pluteus (fig. 224), and the transversely-ringed larvae of Crinoidea (vol. II. fig. 268). The three first of which can be reduced to a common type (fig. 231 c).

ENTEROPNEUSTA. Tornaria (fig. 229).

UROCHORDA (TUNICATA). The tadpole-like larva (vol. in. fig. 8).

GANOIDEI. A larva with a disc with adhesive papillae in front of the mouth (vol. in. fig. 67).

ANUROUS AMPHIBIA. The tadpole (vol. in. fig. 80).



Of the larval forms included in the above list a certain




(After Schultze. )

A. Amphiblastula stage.

B. Stage after the ciliated cells have commenced to be invaginated.

c.s. segmentation cavity; ec. granular epiblast cells; en. ciliated hypoblast cells.

number are probably without affinities outside the group to which they belong. This is the case with the larvae of the



A. Blastosphere stage with hypoblast spheres becoming budded into the central cavity.

B. Planula stage with solid hypoblast.

C. I'lanula stage with a gastric cavity.

</>. epiblast: hy. hypoblast; al. gastric cavity.



Myriapoda, the Crustacean lame, and with the larval forms of the Chordata. I shall leave these forms out of consideration.

There are, again, some larval forms which may possibly turn out hereafter to be of importance, but from which, in the present state of our knowledge, we cannot draw any conclusions. The infusoriform larva of the Dicyemidse, and the Cercaria of the Trematodes, are such forms.

Excluding these and certain other forms, we have finally left for consideration the larvae of the Ccelenterata, the Turbellaria, the Rotifera, the Nemertea, the Mollusca, the Polyzoa, the Brachiopoda, the Chaetopoda, the Gephyrea, the Echinodermata, and the Enteropneusta.

The larvae of these forms can be divided into two groups. The one group contains the larva of the Ccelenterata or Planula, the other group the larvae of all the other forms.

The Planula (fig. 216) is characterised by its extreme simplicity. It is a two-layered organism, with a form varying from cylindrical to oval, and usually a radial symmetry. So long as it remains free it is not usually provided with a mouth, and it is as yet uncertain whether or no the absence of a mouth is to be regarded as an ancestral character. The Planula is very probably the ancestral form of the Ccelenterata.

The larvae of almost all the other groups, although they may be subdivided into a series of very distinct types, yet agree in the possession of certain common characters 1 . There is a more or less dome-shaped dorsal surface, and a flattened or concave ventral surface, containing the open 1 The larva of the Brachiopoda does not possess most of the characters mentioned below. It is probably, all the same, a highly differentiated larval form belonging to this group.




m. mouth ; ms. masticatory apparatus ; me. mesenteron ; an. anus ; Id. lateral gland ; ov. ovary ; t. tail (foot) ; tr. trochal disc ; sg. supraoesophageal ganglion.


ing of the mouth, and usually extending posteriorly to the opening of the anus, when such is present.

The dorsal dome is continued in front of the mouth to form a large prceoral lobe.

There is usually present at first an uniform covering of cilia ; but in the later larval stages there are almost always formed definite bands or rings of long cilia, by which locomotion is effected. These bands are often produced into arm-like processes.

The alimentary canal has, typically, the form of a bent tube with a ventral concavity, constituted (when an anus is present)


(From Lankester.)

/. foot; ol. otocyst; m. mouth; v. velum; ng. nerve ganglion; ry. residual yolk spheres; sAs. shell-gland; i. intestine.

of three sections, viz. an oesophagus, a stomach, and a rectum. The oesophagus and sometimes the rectum are epiblastic in origin, while the stomach always and the rectum usually are derived from the hypoblast 1 .

To the above characters may be added a glass-like transparency ; and the presence of a widish space possibly filled with gelatinous tissue, and often traversed by contractile cells, between the alimentary tract and the body wall.

1 There is some uncertainty as to the development of the oesophagus in the Echinodermata, but recent researches appear to indicate that it is developed from the hypoblast.



Considering the very profound differences which exist between many of these larvae, it may seem that the characters just enumerated are hardly sufficient to justify my grouping them together. It is, however, to be borne in mind that my grounds for doing so depend quite as much upon the fact that A B


A. and B. Earlier and later stage of Gasteropod. C. Pteropod (Cymbulia). v. velum; c. shell; /. foot; op. operculum ; t. tentacle.

they constitute a series without any great breaks in it, as upon the existence of characters common to the whole of them. It is also worth noting that most of the characters which have been enumerated as common to the whole of these larvae are not such secondary characters as (in accordance with the considerations used above) might be expected to arise from the fact of their being subjected to nearly similar conditions of life. Their transparency is, no doubt, such a secondary character, and it is not impossible that the existence of ciliated bands may be so also ; but it is quite possible that if, as I suppose, these larvae reproduce the characters of some ancestral form, this form may have existed at a time when all marine animals were free-swimming, and that it may, therefore, have been provided with at least one ciliated band.

FIG. 220. LARVA OF ARGIOPE. (From Gegenbaur ; after Kowalevsky.)

m. mantle ; b. setre ; d. archenteron.


2 4


The detailed consideration of the characters of these larvae, given below, supports this view.

This great class of larvae may, as already stated, be divided into a series of minor subdivisions. These subdivisions are the following :

1. The Pilidium Group. This group is characterised by the mouth being situated nearly in the centre of the ventral surface, and by the absence of an anus. It includes the Pilidium


(After Metschnikoff.)

ae. archenteron; oe. oesophagus; st. stomach; am. amnion; pr.d. prostomial disc ; pod. metastomial disc ; c.s. cephalic sack (lateral pit).

of the Nemertines (fig. 221), and the various larvae of marine Dendrocoela (fig. 222). At the apex of the praeoral lobe a thickening of epiblast may be present, from which (fig. 232) a contractile cord sometimes passes to the oesophagus.

2. The Echinoderm Group. This group (figs. 223, 224 and 231 C) is characterised by the presence of a longitudinal pastoral band of cilia, by the absence of special sense organs in the praeoral region, and by the development of the body cavity as an outgrowth of the alimentary tract. The three typical divisions of the alimentary tract are present, and there is a more or less developed praeoral lobe. This group only includes the larvae of the Echinodermata.


3. The Trochosphere Group. This group (figs. 225, 226) is characterised by the presence of a praeoral ring of long cilia, the region in front of which forms a great part of the praeoral lobe. The mouth opens immediately behind the praeoral ring of cilia, and there is very often a second ring of short cilia parallel to the main ring, immediately behind the mouth. The



B. MULLER'S TURBELLARIAN LARVA (PROBABLY THYSANOZOON). VIEWED FROM THE VENTRAL SURFACE. (After Muller.) The ciliated band is represented by the black line. m. mouth ; u.l. upper lip.

function of the ring of short cilia is nutritive, in that its cilia are employed in bringing food to the mouth ; while the function of the main ring is locomotive. A perianal patch or ring of cilia is often present (fig. 225 A), and in many forms intermediate rings are developed between the praeoral and perianal rings.

The praeoral lobe is usually the seat of a special thickening of epiblast, which gives rise to the supra-cesophageal ganglion of the adult. On this lobe optic organs are very often developed in connection with the supra-oesophageal ganglion, and a contractile band frequently passes from this region to the oesophagus.

The alimentary tract is formed of the three typical divisions.

The body cavity is not developed directly as an outgrowth of the alimentary tract, though the process by which it originates is very probably secondarily modified from a pair of alimentary outgrowths.

24 2



Paired excretory organs, opening to the exterior and into the body cavity, are often present (fig. 226 nph}.

This type of larva is found in the Rotifera (fig. 217) (in which it is preserved in the adult state), the Chaetopoda (figs. 225 and 226), the Mollusca (fig. 218), the Gephyrea nuda (fig. 227), and the Polyzoa (fig. 228)'.


m. mouth; si. stomach; a. anus; I.e. primitive longitudinal ciliated band; pr.c. pneoral ciliated band.

4. Tornaria. This larva (fig. 229) is intermediate in most of its characters between the larvae of the Echinodermata (more especially the Bipinnaria) and the Trochosphere. It resembles Echinoderm larvae in the possession of a longitudinal ciliated band (divided into a praeoral and a postoral ring), and in the derivation of the body cavity and water-vascular vesicle from alimentary diverticula ; and it resembles the Trochosphere in the presence of sense organs on the praeoral lobe, in the existence of a perianal ring of cilia, and in the possession of a contractile band passing from the praeoral lobe to the oesophagus.


m. mouth : d. stomach ;


a. anus ; o. oesophagus ; c. intestine ; v ' . and v.

ciliated ridges ; w. water- vascular tube ; r. calcareous rods.

1 For a discussion as to the structure of the Polyzoon larva, vide Vol. II. p. 305.


5. Actinotrocha. The remarkable larva of Phoronis (fig. 230), known as Actinotrocha, is characterised by the presence of (i) a postoral and somewhat longitudinal ciliated ring produced into tentacles, and (2) a perianal ring. It is provided with a prseoral lobe, and a terminal or somewhat dorsal anus.

6. The larva of the Brachiopoda articulata (fig. 220). The relationships of the six types of larval forms thus briefly

characterised have been the subject of a considerable amount of controversy, and the following suggestions on their affinities must be viewed as somewhat speculative. The Pilidium type of larva is in some important respects less highly differentiated

FIG. 225. Two CH^TOPOD LARWE. (From Gegenhaur.)

o. mouth ; i. intestine ; a. anus ; v. praeoral ciliated band ; w. perianal ciliated band.

than the larvae of the five other groups. It is, in the first place, without an anus ; and there are no grounds for supposing that the anus has become lost by retrogressive changes. If for the moment it is granted that the Pilidium larva represents more nearly than the larvae of the other groups the ancestral type of larva, what characters are we led to assign to the ancestral form which this larva repeats ?

In the first place, this ancestral form, of which fig. 231 A is an ideal representation, would appear to have had a dome-shaped body, with a flattened oral surface and a rounded aboral surface. Its symmetry was radial, and in the centre of the flattened oral surface was placed the mouth, and round its edge was a ring of cilia. The passage of a Pilidium-like larva into the vermiform bilateral Platyelminth form, and therefore it may be presumed of the ancestral form which this larva repeats, is effected by the


larva becoming more elongated, and by the region between the mouth and one end of the body becoming the pneoral region, and by an outgrowth between the mouth and the opposite end developing into the trunk, an anus becoming placed at its extremity in the higher forms.

If what has been so far postulated is correct, it is clear that this primitive larval form bears a very close resemblance to a simplified free-swimming Ccelenterate (Medusa), and that the conversion of such a radiate form into

..... , , , , . , , i FlG. 226. POLYGORDIUS

the bilateral took place, not by the LARVA- ( After Hatschek.) elongation of the aboral surface, and ;;/ mouth; ^ ^.^

the formation of an anus there, but by phageal ganglion ; nph. nephri, , , . r . 1 i r dion ; me.p. mesoblastic band :

the unequal elongation of the oral face, aw< anus f oL stomach .

an anterior part, together with the dome

above it, forming a praeoral lobe, and a posterior outgrowth the

trunk (figs. 226 and 233) ; while the aboral surface became the

dorsal surface.

This view fits in very well with the anatomical resemblances between the Coelenterata and the Turbellaria 1 , and shews, if true, that the ventral and median position of the mouth in many Turbellaria is the primitive one.

The above suggestion as to the mode of passage from the radial into the bilateral form differs largely from that usually held. Lankester 2 , for instance, gives the following account of this passage :

" It has been recognised by various writers, but notably by Gegenbaur and Haeckel, that a condition of radiate symmetry must have preceded the condition of bilateral symmetry in animal evolution. The Diblastula may be conceived to have been at first absolutely spherical with spherical symmetry. The establishment of a mouth led necessarily to the establishment of a structural axis passing through the mouth, around which axis the body was arranged with radial symmetry. This condition is more or less perfectly maintained by many Ccelenterates, and is reassumed by degrada 1 Vide Vol. II. pp. 179 and 191. In this connection attention may be called to Cceloplana Mdschnikowii, a form described by Kowalevsky, Zoologischer Anzeiger, No. 52, p. 140, as being intermediate between the Ctenophora and the Turbellaria. As already mentioned, there does not appear to me to be sufficient evidence to prove that this form is not merely a creeping Ctenophor.

Qiiart. Journ. of Micr. Science, Vol. XVH. pp. 422-3.



tion of higher forms (Echinoderms, some Cirrhipedes, some Tunicates). The next step is the differentiation of an upper and a lower surface in

FIG. 227. LARVA OF ECHIURUS. (After Salensky.)

  1. . mouth ; an. anus ; sg. supra-oesophageal ganglion (?).

relation to the horizontal position, with mouth placed anteriorly, assumed by the organism in locomotion. With the differentiation of a superior and inferior surface, a right and a left side, complementary one to the other, are necessarily also differentiated. Thus the organism becomes bilaterally symmetrical. The Ccelentera are not wanting in indications of this bilateral symmetry, but for all other higher groups of animals it is a fundamental character. Probably the development of a region in front of, and dorsal to the mouth, forming the Prattomium, was accomplished pari passu with the development of bilateral symmetry. In the radially symmetrical Ccelentera we find very commonly a series of lobes of the bodywall or tentacles produced equally with radial symmetry, that is to say all round the mouth, the mouth terminating the main axis of the body that is to say, the organism being ' telostomiate.' The later fundamental form, common to all animals above the Ccelentera, is attained by shifting what was the main axis of the body so that it may be described now as the ' enteric ' axis ; whilst the new main axis, that parallel with the plane of progression, passes through the dorsal region of the body running obliquely in relation to the enteric axis. Only one lobe or outgrowth of those radially disposed in the telostomiate organisms now persists. This lobe lies dorsally to the mouth, and through it runs the new main axis. This lobe is the Prostomium, and all the organisms which thus develop a new main axis, oblique to the old main axis, may be called prostomiate."



m. mouth ; an. anus ; st. stomach; s. ciliated disc.



It will be seen from this quotation that the aboral part of the body is supposed to elongate to form the trunk, while the prasoral region is derived from one of the tentacles.

Before proceeding to further considerations as to the origin of the Bilateralia, suggested by the Pilidium type of larva, it is necessary to enter into a more detailed comparison between our larval forms.

A very superficial consideration of the characters of these forms brings to light two important features in which they differ, viz. :

(l) In the presence or absence of sense organs on the prasoral lobe.


(After Metschnikoff.)

The black lines represent the ciliated bands.

in. mouth; an. anus; br. branchial cleft; ht. heart; c. body cavity between splanchnic and somatic mesoblast layers ; w. so-called water-vascular vesicle ; v. circular blood-vessel.

(2) In the presence or absence of outgrowths from the alimentary tract to form the body cavity.

The larvae of the Echinodermata and Actinotrocha (?) are without sense organs on the praeoral lobe, while the other types



of larvae are provided with them. Alimentary diverticula are characteristic of the larvae of the Echinodermata and of Tornaria.

If the conclusion already arrived at to the effect that the prototype of the six larval groups was descended from a radiate ancestor is correct, it appears to follow that the nervous system, in so far as it was differentiated, had primitively a radiate form ; and it is also probably true that there were alimentary diverticula in the form of radial pouches, two of which may have given origin to the paired diverticula which become the body cavity in such types as the Echinodermata, Sagitta, etc. If these two points are granted, the further conclusions seem to follow (i) that the ganglion and sense organs of the praeoral lobe were secondary structures, which arose (perhaps as differentiations of an original circular nerve ring) after the assumption of a bilateral form; and (2) that the absence of these organs in the larvae of the Echinodermata and Actinotrocha (?) implies that these larvae retain, so far, more primitive characters than the Pilidium. The same may be said of the alimentary diverticula. There are thus indications that in two important points the Echinoderm larvae are more primitive than the Pilidium.

The above conclusions with reference to the Pilidium and Echinoderm larvae involve some not inconsiderable difficulties, and suggest certain points for further discussion.

In the first place it is to be noted that the above speculations render it probable that the type of nervous system from which that found in the adults of the Echinodermata, Platyelminthes, Chsetopoda, Mollusca, etc., is derived, was a circumoral ring, like that of Medusae, with which radially arranged sense organs may have been connected ; and that in the Echinodermata this form of nervous system has been retained, while in the other types it has been modified. Its anterior part may have given rise to supra-cesophageal ganglia and organs of vision ; these being

FIG. 230. ACTINOTROCHA. (After Metschnikoff.)

/. mouth ; an. anus.



developed on the assumption of a bilaterally symmetrical form, and the consequent necessity arising for the sense organs to be situated at the anterior end of the body. If this view is correct, the question presents itself as to how far the posterior part of the nervous system of the Bilateralia can be regarded as derived from the primitive radiate ring.



A. Ideal ancestral larval form.

B. Larval form from which the Trochosphere larva may have been derived.

C. Larval form from which the typical Echinoderm larva may have been derived.

m. mouth ; an. anus ; st. stomach ; s.g. supra-cesophageal ganglion. The black lines represent the ciliated bands.

A circumoral nerve-ring, if longitudinally extended, might give rise to a pair of nerve-cords united in front and behind exactly such a nervous system, in fact, as is present in many Nemertines 1 (the Enopla and Pelagonemertes), in Peripatus 2 , and in primitive molluscan types (Chiton, Fissurella, etc.). From the lateral parts of this ring it would be easy to derive the ventral cord of the Chaetopoda and Arthropoda. It is especially deserving of notice in connection with the nervous system of the

1 Vute Hubrecht, "Zur Anat. und Phys. d. Nerven-System. d. Nemertinen," Kbn. Akad. Wiss., Amsterdam ; and " Researches on the Nervous System of Nemertines," Quart. Journ. of Micr. Science, 1880.

  • Vide F. M. Balfour, " On some points in the Anat. of Peripatus capensis," Quart.

Jourt:. of Micr. Science, Vol. xix. 1879.


above-mentioned Nemertines and Peripatus, that the commissure connecting the two nerve-cords behind is placed on the dorsal side of the intestine. As is at once obvious, by referring to the diagram (fig. 231 B), this is the position this commissure ought, undoubtedly, to occupy if derived from part of a nerve-ring which originally followed more or less closely the ciliated edge of the body of the supposed radiate ancestor.

The fact of this arrangement of the nervous system being found in so primitive a type as the Nemertines tends to establish the views for which I am arguing ; the absence or imperfect development of the two longitudinal cords in Turbellarians may very probably be due to the posterior part of the nerve-ring having atrophied in this group.

It is by no means certain that this arrangement of the nervous system in some Mollusca and in Peripatus is primitive, though it may be so.

In the larvae of the Turbellaria the development of sense organs in the praeoral region is very clear (fig. 222 B) ; but this is by no means so obvious in the case of the true Pilidium. There is in Pilidium (fig. 232 A) a thickening of epiblast at the summit of the dorsal dome, which might seem, from the analogy of Mitraria, etc. (fig. 233), to correspond to the thickening of the praaoral lobe, which gives rise to the supra-cesophageal ganglion ; but, as a matter of fact, this part of the larva does not apparently enter into the formation of the young Nemertine (fig. 232). The peculiar metamorphosis, which takes place in the development of the Nemertine out of the Pilidium 1 , may, perhaps, eventually supply an explanation of this fact ; but at present it remains as a still unsolved difficulty.

The position of the flagellum in Pilidium, and of the supra-cesophageal ganglion in Mitraria, suggests a different view of the origin of the supraoesophageal ganglion from that adopted above. The position of the ganglion in Mitraria corresponds closely with that of the auditory organ in Ctenophora ; and it is not impossible that the two structures may have had a common origin. If this view is correct, we must suppose that the apex of the aboral lobe has become the centre of the praeoral field of the Pilidium and Trochosphere larval forms 2 a view which fits in very well with their structure (figs. 226 and 233). The whole of the questions concerning the nervous system are still very obscure, and until further facts are brought to light no definite conclusions can be arrived at.

1 Vide Vol. ii. p. 204.

2 The independent development of the supra-cesophageal ganglion and ventral nerve-cord in Chaetopoda (vide Kleinenberg, Development of Lumbricus trapezoides) agrees very satisfactorily with this view.


The absence of sense organs on the praeoral lobe of larval Echinodermata, coupled with the structure of the nervous system of the adult, points to the conclusion that the adult Echinoder


ft. oesophagus ; st. stomach ; i. intestine ; fr. proboscis ; lp. lateral pit (cephalic sack) ; a. amnion ; n. nervous system.

mata have retained, and not, as is now usually held, secondarily acquired, their radial symmetry; and if this is admitted it follows that the obvious bilateral symmetry of Echinoderm larvae is a secondary character.

The bilateral symmetry of many Ccelenterate larvae (the larva of ,/Eginopsis, of many Acraspeda, of Actinia, &c.), coupled with the fact that a bilateral symmetry is obviously advanta


geous to a free-swimming form, is sufficient to shew that this supposition is by no means extravagant ; while the presence of only two alimentary diverticula in Echinoderm larvae is quite in accord with the presence of a single pair of perigastric chambers in the early larva of Actinia, though it must be admitted that the derivation of the water-vascular system from the left diverticulum is not easy to understand on this view.

A difficulty in the above speculation is presented by the fact of the anus of the Echinodermata being the permanent blastopore, and arising prior to the mouth. If this fact has any special significance, it becomes difficult to regard the larva of Echinoderms and that of the other types as in any way related ; but if the views already urged, in a previous section on the germinal layers, as to the unimportance of the blastopore, are admitted, the fact of the anus coinciding with the blastopore ceases to be a difficulty. As may be seen, by referring to fig. 231 C, the anus is placed on the dorsal side of the ciliated band. This position for the anus adapts itself to the view that the Echinoderm larva had originally a radial symmetry, with the anus placed at the aboral apex, and that, with the elongation of the larva on the attainment of a bilateral symmetry, the aboral apex became shifted to the present position of the anus.

It may be noticed that the obscure points connected with the absence of a body cavity in most adult Platyelminthes, which have already been dealt with in the section of this chapter devoted to the germinal layers, present themselves again here ; and that it is necessary to assume either that alimentary diverticula, like those in the Echinodermata, were primitively present in the Platyelminthes, but have now disappeared from the ontogeny of this group, or that the alimentary diverticula have not become separated from the alimentary tract.

So far the conclusion has been reached that the archetype of the six types of larvae had a radiate form, and that amongst existing larvae it is most nearly approached in general shape and in the form of the alimentary canal by the Pilidium group, and in certain other particulars by the Echinoderm larvae.

The edge of the oral disc of the larval archetype was probably armed with a ciliated ring, from which the ciliated ring of the Pilidium type and of the Echinodermata was most likely derived. The ciliated ring of the Pilidium varies greatly in its characters,


and has not always the form of a complete ring. In Pilidium proper (fig. 232 A) it is a simple ring surrounding the edge of the oral disc. In Muller's larva of Thysanozoon (fig. 222 B) it is

FlG. 233. TWO STAGES IN THE DEVELOPMENT OF MlTRARIA. (After Metschnikoff.) m. mouth; an. anus; sg. supra-cesophageal ganglion; br. and b. provisional bristles ; pr.b. prasoral ciliated band.

inclined at an axis to the oral disc, and might be called praeoral, but such a term cannot be properly used in the absence of an anus.


m. mouth ; a '. anus ; f.g. foot gland ; x. problematical body (probably a bud).

The aboral apex is turned downwards.


The Echinoderm ring is oblique to the axis of the body, and, owing to the fact of its passing ventrally in front of the anus, must be called postoral.

The next point to be considered is that of the affinities of the other larval types to these two types.

The most important of all the larval types is the Trochosphere, and this type is undoubtedly more closely related to the Pilidium than to the Echinoderm larva. Mitraria amongst the Chaetopods (fig. 233) has, indeed, nearly the form of a Pilidium, and mainly differs from a Pilidium in the possession of an anus and of provisional bristles ; the same may be said of Cyphonautes (fig. 234) amongst the Polyzoa.

The existence of these two forms appears to shew that the praeoral ciliated ring of the Trochosphere may very probably be derived directly from the circumoral ciliated ring of the Pilidium; the other ciliated rings or patches of the Trochosphere having a secondary origin.

The larva of the Brachiopoda (fig. 220), in spite of its peculiar characters, is, in all probability, more closely related to the Chaetopod Trochosphere than to any other larval type. The most conspicuous point of agreement between them is, however, the possession in common of provisional setae.

Echinoderm larvae differ from the Trochosphere, not only in the points already alluded to, but in the character of the ciliated band. The Echinoderm band is longitudinal and postoral. As just stated, there is reason to think that the praeoral band of the Trochosphere and the postoral band of the Echinoderm larva are both derived from a ciliated ring surrounding the oral disc of the prototype of these larvae (vide fig. 231). In the case of the Echinodermata the anus must have been formed on the dorsal side of this ring, and in the case of the Trochosphere on the ventral side ; and so the difference in position between the two rings was brought about. Another view with reference to these rings has been put forward by Gegenbaur and Lankester, to the effect that the praeoral ring of the Trochosphere is derived from the breaking up of the single band of most Echinoderm larvae into the two bands found in Bipinnaria (vide fig. 223) and the atrophy of the posterior band. There is no doubt a good deal to be said for this origin of the praeoral ring, and it is


strengthened by the case of Tornaria ; but the view adopted above appears to me more probable.

Actinotrocha (fig. 230) undoubtedly resembles more closely Echinoderm larvae than the Trochosphere. Its ciliated ring has Echinoderm characters, and the growth along the line of the ciliated ring of a series of arms is very similar to what takes place in many Echinoderms. It also agrees with the Echinoderm larvae in the absence of sense organs on the praeoral lobe.

Tornaria (fig. 229) cannot be definitely united either with the Trochosphere or with the Echinoderm larval type. It has important characters in common with both of these groups, and the mixture of these characters renders it a very striking and well-defined larval form.

Phylogenetic conclusions. The phylogenetic conclusions which follow from the above views remain to be dealt with. The fact that all the larvae of the groups above the Ccelenterata can be reduced to a common type seems to indicate that all the higher groups are descended from a single stem.

Considering that the larvae of comparatively few groups have persisted, no conclusions as to affinities can be drawn from the absence of a larva in any group; and the presence in two groups of a common larval form may be taken as proving a common descent, but does not necessarily shew any close affinity.

There is every reason to believe that the types with a Trochosphere larva, viz. the Rotifera, the Mollusca, the Chaetopoda, the Gephyrea, and the Polyzoa, are descended from a common ancestral form ; and it is also fairly certain there was a remote ancestor common to these forms and to the Platyelminthes. A general affinity of the Brachiopoda with the Chaetopoda is more than probable. All these types, together with various other types which are nearly related to them, but have not preserved an early larval form, are descended from a bilateral ancestor. The Echinodermata, on the other hand, are probably directly descended from a radial ancestor, and have more or less completely retained their radial symmetry. How far Actinotrocha 1 is related to the Echinoderm larvae cannot be settled. Its characters may possibly be secondary, like those of the

1 It is quite possible that Phoronis is in no way related to the other Gephyrea.


mesotrochal larvae of Chaetopods, or they may be due to its having branched off very early from the stock common to the whole of the forms above the Ccelenterata. The position of Tornaria is still more obscure. It is difficult, in the face of the peculiar water-vascular vesicle with a dorsal pore, to avoid the conclusion that it has some affinities with the Echinoderm larvae. Such affinities would seem, on the lines of speculation adopted in this section, to prove that its affinities to the Trochosphere, striking as they appear to be, are secondary and adaptive. From this conclusion, if justified, it would follow that the Echinodermata and Enteropneusta have a remote ancestor in common, but not that the two groups are in any other way related.

General conclusions and summary. Starting from the demonstrated fact that the larval forms of a number of widely separated types above the Ccelenterata have certain characters in common, it has \&&\ provisionally assumed that the characters have been inherited from a common ancestor ; and an attempt has been made to determine (i) the characters of the prototype of all these larvae, and (2) the mutual relations of the larval forms in question. This attempt started with certain more or less plausible suggestions, the truth of which can only be tested by the coherence of the results which follow from them, and their capacity to explain all the facts.

The results arrived at may be summarised as follows :

1. The larval forms above the Ccelenterata may be divided into six groups enumerated on pages 370 to 373.

2. The prototype of all these groups was an organism something like a Medusa, with a radial symmetry. The mouth was placed in the centre of a flattened ventral surface. The aboral surface was dome-shaped. Round the edge of the oral surface was a ciliated ring, and probably a nervous ring provided with sense organs. The alimentary canal was prolonged into two or more diverticula, and there was no anus.

3. The bilaterally symmetrical types were derived from this larval form by the larva becoming oval, and the region in front of the mouth forming a praeoral lobe, and that behind the mouth growing out to form the trunk. The aboral dome became the dorsal surface.

On the establishment of a bilateral symmetry the anterior

15. in. 25


part of the nervous ring gave rise (?) to the supra-cesophageal ganglia, and the optic organs connected with them ; while the posterior part of the nerve-ring formed (?) the ventral nerve-cords. The body cavity was developed from two of the primitive alimentary diverticula.

The usual view that radiate forms have become bilateral by the elongation of the aboral dome into the trunk is probably erroneous.

4. Pilidium is the larval form which most nearly reproduces the characters of the larval prototype in the course of its conversion into a bilateral form.

5. The Trochosphere is a completely differentiated bilateral form, in which an anus has become developed. The praeoral ciliated ring of the Trochosphere is probably directly derived from the ciliated ring of Pilidium, which is itself the original ring of the prototype of all these larval forms.

6. Echinoderm larvae, in the absence of a nerve-ganglion or special organs of sense on the prseoral lobe, and in the presence of alimentary diverticula, which give rise to the body cavity, retain some characters of the prototype larva which have been lost in Pilidium. The ciliated ring of Echinoderm larvae is probably derived directly from that of the prototype by the formation of an anus on the dorsal side of the ring. The anus was very probably originally situated at the aboral apex.

Adult Echinoderms have probably retained the radial symmetry of the forms from which they are descended, their nervous ring being directly derived from the circular nervous ring of their ancestors. They have not, as is usually supposed, secondarily acquired their radial symmetry. The bilateral symmetry of the larva is, on this view, secondary, like that of so many Coelenterate larvae.

7. The points of similarity between Tornaria and (i) the Trochosphere and (2) the Echinoderm larvae are probably adaptive in the one case or the other ; and, while there is no difficulty in believing that those to the Trochosphere are adaptive, the presence of a water- vascular vesicle with a dorsal pore renders probable a real affinity with Echinoderm larvae.

8. It is not possible in the present state of our knowledge to decide how far the resemblances between Actinotrocha and Echinoderm larvae are adaptive or primary.



(257) Allen Thomson. British Association Address, 1877.

(258) A. Agassiz. " Embryology of the Ctenophorae." Mem. Amer. Acad. of Arts and Sciences, Vol. X. 1874.

(259) K. E. von Baer. Ueb. Entivicklungsgeschichte d. Thiere. Konigsberg, 18281837.

(260) F. M. Balfour. "A Comparison of the Early Stages in the Development of Vertebrates." Quart. Joum. of Micr. Set., Vol. XV. 1875.

(261) C. Glaus. Die Typenlehre u. E. HaeckeFs sg. Gastraa-tlieorie. Wien, 1874.

'(262) C. Glaus. Grundziige d. Zoologie. Marburg und Leipzig, 1879.

(263) A. Dohrn. Der Ursprung d. Wirbelthiere u. d. Princip des Functionsivechsels. Leipzig, 1875.

(264) C. Gegenbaur. Grttndriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also Translation. Elements of Comparative Anatomy. Macmillan & Co. 1878.

(265) A. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1874.

(266) E. Haeckel. Studien z. Gastraa-theorie, Jena, 1877; and also jtenaisc/ic Zeitschrift, Vols. vin. and IX. 1874-5.

(267) E. Haeckel. Schopfungsgeschichte. Leipzig. Vide also Translation, The History of Creation. King & Co., London, 1878.

(268) E. Haeckel. Anthropogenic. Leipzig. Vide also Translation, Anthropogeny. Kegan Paul & Co., London, 1878.

(269) B. Hatschek. "Studien lib. Entwicklungsgeschichte d. Anneliden." Arbeit, a. d. zool. Instit. d. Univer. Wien. 1878.

(270) O. and R. Hertwig. "Die Actinien." Jenaische Zeitschrift, Vols. xm. and xiv. 1879.

(271) O. and R. Hertwig. Die Ccelomtheorie. Jena, 1881'.

(272) O. Hertwig. Die Chatognathen. Jena, 1880.

(273) R. Hertwig. Ueb. d. Bau d. Ctenophoren. Jena, 1880.

(274) T. H. Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.

(274*) T. H. Huxley. "On the Classification of the Animal Kingdom." Quart. J. of Micr. Science, Vol. xv. 1875.

(275) N. Kleinenberg. Hydra, eine anatomisch-cntwickhingsgeschichtiiche Untersuchung. Leipzig, 1872.

(276) A. Kolliker. Entwicklungsgeschichte d. Menschen it, d. hoh. Thiere. Leipzig, 1879.

(277) A. Kowale vsky. " Embryologische Studien an Wiirmern u. Arthropoden." Mem. Acad. Petersbourg, Series vil. Vol. xvi. 1871.

(278) E. R. Lankester. "On the Germinal Layers of the Embryo as the Basis of the Genealogical Classification of Animals." Ann. and Mag. of Nat. Hist. 1873 1 This important memoir only came into my hands after this chapter was already in type.

25 2


(279) E. R. Lankester. "Notes on Embryology and Classification." Quart. Jonrn. of Micr. Set., Vol. XVII. 1877.

(280) E. Metschnikoff. "Zur Entwicklungsgeschichte d. Kalkschwamme." Zeit.f. wiss. Zool., Vol. xxiv. 1874.

(281) E. Metschnikoff. " Spongiologische Stuclien." Zeit.f, wiss. Zool., Vol. xxxn. 1879.

(282) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative Embryology. Holt and Co., New York, 1876.

(283) C. Rabl. " Ueb. d. Entwick. d. Malermuschel. " Jenaische Zeitsch., Vol. x. 1876.

(284) C. Rabl. "Ueb. d. Entwicklung. d. Tellerschnecke (Planorbis)." Morph. Jahrbuch, Vol. v. 1879.

(285) H. Rathke. Abhandlungen 2. Bildung und Entwicklungsgesch. d. Menschen . d. Thiere. Leipzig, 1833.

(286) H. Rathke. Ueber die Bildung u. Entwicklungs. d. Flusskrebses. Leipzig, 1829.

(287) R. Remak. Untersuch. iib. d. Entwick. d. Wirbelthiere. Berlin, 1855.

(288) Salensky. " Bemerkungen iib. Haeckels Gastrsea-theorie." Archiv f. Na turgesch ich te, 1874.

(289) E. Schafer. "Some Teachings of Development." Quart. Jonnt. of Micr. Science, Vol. xx. 1880.

(290) C. Semper. "Die Verwandtschaftbeziehungen d. gegliederten Thiere. Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. III. 1876-7.





OUR knowledge of the development of the organs in most of the Invertebrate groups is so meagre that it would not be profitable to attempt to treat systematically the organogeny of the whole animal kingdom.

For this reason the plan adopted in this section of the work has been to treat somewhat fully the organogeny of the Chordata, which is comparatively well known ; and merely to indicate a few salient facts with reference to the organogeny of other groups. In the case of the nervous system, and of some other organs which especially lend themselves to this treatment, such as the organs of special sense and the excretory system, a wider view of the subject has been taken ; and certain general principles underlying the development of other organs have also been noticed.

The classification of the organs is a matter of some difficulty. Considering the character of this treatise it seemed desirable to arrange the organs according to the layers from which they are developed. The compound nature of many organs, e.g. the eye and ear, renders it, however, impossible to carry out consistently such a mode of treatment. I have accordingly adopted a rough classification of the organs according to the layers, dropping the principle where convenient, as, for instance, in the case of the stomodaeum and proctodseum.

The organs which may be regarded as mainly derived from


the epiblast are (i) the skin; (2) the nervous system; (3) the organs of special sense.

Those from the mesoblast are (i) the general connective tissue and skeleton ; (2) the vascular system and body cavity ; (3) the muscular system ; (4) the urinogenital system.

Those from the hypoblast are the alimentary tract and its derivates ; with which the stomodaeum and proctodaeum and their respective derivates are also dealt with.


General works dealing with the development of the organs of the


(291) K. E. von Baer. Ueber Entwicklungsgeschichte d. Thiere. Konigsberg, 18281837.

(292) F. M. Balfour. A Monograph on tlic development of Elasmobrancli Fishes. London, 1878.

(293) Th. C. W. Bischoff. Entwicklungsgesch. d. Sdtigethiere ti. d. Menschen. Leipzig, 1842.

(294) C. Gegenbaur. Gnindriss d. vergleichenden Anatomic. Leipzig, 1878. Vide also English translation, Elements of Comp. Anatomy. London, 1878.

(295) M. Foster and F. M. Balfour. The Elements of Embryology. Part I. London, 1874.

(296) Alex. Gotte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(297) W. His. Untersitch. iib. d. erste Anlage d. Wirbelthierleibcs . Leipzig, 1868.

(298) A. Ko Hiker. Entwicklungsgeschichte d. Menschen u. der hoheren Thiere. Leipzig, 1879.

(299) H. Rathke. Abhandlungen it. Bildung mid Entwicklungsgeschichle d. Menschen it. d. Thiere. Leipzig, 1838.

(300) H. Rathke. Entwicklungs. d. Natter. Kbnigsberg, 1839.

(301) H. Rathke. Entwicklungs. d. Wirbelthiere. Leipzig, 1861.

(302) R. Remak. Untersuchnngen iib. d. Entwicklung d. Wirbelthiere. Berlin, 18501855.

(303) S. L. Schenk. Lehrbuch d. vei'gleich. Embryologie d. Wirbeltliicre. Wien, 1874.