The Works of Francis Balfour 1-14
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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.
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Vol I. Separate Memoirs (1885)
XIV. On the Early Development of the Lacertilia, together with some Observations on the Nature and relations of the Primitive Streak
(With Plate 29.)
TILL quite recently no observations were recorded on the early developmental changes of the reptilian ovum. Not long ago Professors Kupffer and Benecke published a preliminary note on the early development of Lacerta agilis and Emys Europea*. I have myself also been able to make some observations on the embryo of Lacerta muralis. The number of my embryos has been somewhat limited, and most of those which I have had have been preserved in bichromate of potash, which has turned out a far from satisfactory hardening reagent. In spite of these difficulties I have been led on some points to very different results from those of the German investigators, and to results which are more in accordance with what we know of other Sauropsidan types. I commence with a short account of the results of Kupffer and Benecke.
Segmentation takes place exactly as in birds, and the resulting blastoderm, which is thickened at its edge, spreads rapidly over the yolk. Shortly before the yolk is half enclosed a small embryonic shield (area pellucida) makes its appearance in the centre of the blastoderm, which has, in the meantime, become divided into two layers. The upper of these is the epiblast, and the lower the hypoblast. The embryonic shield is mainly distinguished from the remainder of the blastoderm by the more columnar character of its constituent epiblast cells. It is somewhat pyriform in shape, the narrower end corresponding with
1 From the Quarterly Journal of Microscopical Science, Vol. XIX. 1879.
2 Die Erste Entwieklungsvorgangc am Ei der Replilien, Konigsberg, 1878.
EARLY DEVELOPMENT OF THE LACERTILIA. 645
the future posterior end of the embryo. At the narrow end an invagination takes place, which gives rise to an open sac, the blind end of which is directed forwards. The opening of this sac is regarded by the authors as the blastopore. A linear thickening of epiblast arises in front of the blastopore, along the median line of which the medullary groove soon appears. In the caudal region the medullary folds spread out and enclose between them the blastopore, behind which they soon meet again. On the conversion of the medullary groove into a closed canal the blastopore becomes obliterated. The mesoblast grows out from the lip of the blastopore as four masses. Two of these are lateral: a third is anterior and median, and, although at first independent of the epiblast, soon attaches itself to it, and forms with it a kind of axis-cord. A fourth mass applied itself to the walls of the sac formed by invagination.
With reference to the very first developmental phenomena my observations are confined to two stages during the segmentation 1 . In the earliest of these the segmentation was about half completed, in the later one it was nearly over. My observations on these stages bear out generally the statements of Kupffer and Benecke. In the second of them the blastoderm was already imperfectly divided into two layers a superficial epiblastic layer formed of a single row of cells, and a layer below this several rows deep. Below this layer fresh segments were obviously being added to the blastoderm from the subjacent yolk.
Between the second of these blastoderms and my next stage there is a considerable gap. The medullary plate is just established, and is marked by a shallow groove which becomes deeper in front. A section through the embryo is represented in PL 29, Series A, fig. I. In this figure there may be seen the thickened medullary plate with a shallow medullary groove, below which are two independent plates of mesoblast (me. p.}, one on each side of the middle line, very imperfectly divided into somatopleuric and splanchnopleuric layers. Below the mesoblast is a continuous layer of hypoblast (/y.), which develops a rod-like thickening along the axial line (ch.} . This rod becomes in the next .stage the notochord. Although this embryo is not well
1 For these two specimens, which were hardened in picric acid, I am indebted to Dr Kleinenberg.
646 EARLY DEVELOPMENT OF THE LACERTILIA.
preserved I feel very confident in asserting the continuity of the notochord with the hypoblast at this stage.
At the hind end of the embryo is placed a thickened ridge of tissue which continues the embryonic axis. In this ridge all the layers coalesce, and I therefore take it to be equivalent to the primitive streak of the avian blastoderm. It is somewhat triangular in shape, with the apex directed backward, the broad base placed in front.
At the junction between the primitive streak and the blastoderm is situated a passage, open at both extremities, leading from the upper surface of the blastoderm obliquely forwards to the lower.
The dorsal and anterior wall of this passage is formed of a distinct epithelial layer, continuous at its upper extremity with the epiblast, and at its lower with the notochordal plate, so that it forms a layer of cells connecting together the epiblast and hypoblast. The hinder and lower wall of the passage is formed by the cells of the primitive streak, which only assume a columnar form near the dorsal opening of the passage (vide fig. 4). This passage is clearly the blind sac of Kupffer and Benecke, who, if I am not mistaken, have overlooked its lower opening. As I hope to show in the sequel, it is also the equivalent of the neurenteric passage, which connects the neural and alimentary canals in the Ichthyopsida, and therefore represents the blastopore of Amphioxus, Amphibians, &c.
Series A, figs. 2, 3, 4, 5, illustrate the features of the passage and its relation to the embryo.
Fig. 2 passes through the ventral opening of the passage. The notochordal plate (ck'.} is vaulted over the opening, and on the left side is continuous with the mesoblast as well as the hypoblast. Figs. 3 and 4 are taken through the middle part of the passage (ne.), which is bounded above by a continuation of the notochordal plate, and below by the tissue of the primitive streak. The hypoblast (/y.),. in the middle line, is imperfectly fused with the mesoblast of the primitive streak, which is now continuous across the middle line. The medullary groove has disappeared, but the medullary plate (m p.) is quite distinct,
In fig. 5 is seen the dorsal opening of the passage (ne,). If a section behind this had been figured, as is done for the next
EARLY DEVELOPMENT OF THE LACERTILIA. 647
series (B), it would have passed through the primitive streak, and, as in the chick, all the layers would have been fused together. The epiblast in the primitive streak completely coalesces with the mesoblast; but the hypoblast, though attached to the other layers in the middle line, can always be traced as a distinct stratum.
Fig. B is a surface view of my next oldest embryo. The medullary groove has become much deeper, especially in front. Behind it widens out to form a space equivalent to the sinus rhomboidalis of the embryo bird. The amnion forms a small fold covering over the cephalic extremity of the embryo, which is deeply embedded in the yolk. Some somites (protovertebrae) were probably present, but this could not be made out in the opaque embryo.
The woodcut (fig. i) represents a diagrammatic longitudinal section through this embryo, and the sections belonging to
FlG. i. Diagrammatic longitudinal section of an embryo of Lacerta. //. Body cavity, am. Amnion. ne. Neurenteric canal, ch. Notochord. hy. Hypoblast. ep. Epiblast. pr. Primitive streak.
Series B illustrate the features of the hind end of the embryo and of the primitive streak.
As is shown in fig. i, the notochord (c/t.) has now throughout the region of the embryo become separated from the subjacent hypoblast, and the lateral plates of mesoblast are distinctly divided into somatic and splanchnic layers. The medullary groove is continued as a deepish groove up to the opening of the neurenteric passage, which thus forms a perforation in the floor of the hinder end of the medullary groove (vide Series B, figs. 2, 3, and 4).
The passage itself is somewhat shorter than in the previous stage, and the whole of it is shown in a single section (fig. 4). This section must either have been taken somewhat obliquely,
648 EARLY DEVELOPMENT OF THE LACERTILIA.
or else the passage have been exceptionally short in this embryo, since in an older embryo it could not all be seen in one section. The front wall of the passage is continuous with the notochord, which for two sections or so in front remains attached to the hypoblast (figs. 2 and 3). Behind the perforation in the floor of the medullary groove is placed the primitive streak (fig. 5), where all the layers become fused together, as in the earlier stage. Into this part a narrow diverticulum from the end of the medullary groove is continued for a very short distance (vide
fig. 5, **.)
The general features of the stage will best be understood by an examination of the diagrammatic longitudinal section, represented in woodcut, fig. I. In front is shown the amnion (am.), growing over the head of the embryo. The notochord (c/i.) is seen as an independent cord for the greater part of the length of the embryo, but falls into the hypoblast shortly in front of the neurenteric passage. The neurenteric passage is shown at ne. t and behind it is shown the primitive streak.
In a still older stage, represented in surface view on PL 29, fig. C, the medullary folds have nearly met above, but have not yet united. The features of the passage from the neural groove to the hypoblast are precisely the same in the embryo just described, although the lumen of the passage has become somewhat narrower. There is still a short primitive streak behind the embryo.
The neurenteric passage persists but a very short time after the complete closure of the medullary canal. It is in no way connected with the allantois, as conjectured by Kupffer and Benecke, but the allantois is formed, as I have satisfied myself by longitudinal sections of a later stage, in the manner already described by Dobrynin, Gasser, and Kolliker for the bird and mammal.
The general results of Kupffer's and Benecke's observations, with the modifications introduced by my own observations, are as follows : After the segmentation and the formation of the embryonic shield (area pellucida) the blastoderm becomes distinctly divided into epiblast and hypoblast 1 . At the hind end of the shield a somewhat triangular primitive streak is formed by
1 This appears to me to take place before the formation of the embryonic shield.
EARLY DEVELOPMENT OF THE LACERT1LIA. 649
the fusion of the epiblast and hypoblast with a number of cells between them, which are probably derived from the lower rows of the segmentation cells. At the front end of the streak a passage arises, open at both extremities, leading obliquely forwards through the epiblast to the space below the hypoblast. The walls of the passage are formed of a layer of columnar cells continuous both with epiblast and hypoblast. In front of the primitive streak the body of the embryo becomes first differentiated by the formation of a medullary plate, and at the same time there grows out from the primitive streak a layer of mesoblast, which spreads out in all directions between the epiblast and hypoblast. In the axis of the embryo the mesoblast plate is stated by Kupffer and Benecke to be continuous across the middle line, but this appears very improbable. In a slightly later stage the medullary plate becomes marked by a shallow groove, and the mesoblast of the embryo is then undoubtedly constituted of two lateral plates, one on each side of the median line. In the median line the notochord arises as a ridge-like thickening of the hypoblast, which becomes very soon quite separated from the hypoblast, except at the hind end, where it is continued into the front wall of the neurenteric passage. It is interesting to notice the remarkable relation of the notochord to the walls of the neurenteric passage. More or less similar relations are also well marked in the case of the goose and the fowl (Gasser) 1 , and support the conclusion deducible from the lower forms of vertebrata, that the notochord is essentially hypoblastic.
The passage at the front end of the primitive streak forms the posterior boundary of the medullary plate, though the medullary groove is not at first continued back to it. The anterior wall of this passage connects together the medullary plate and the notochordal ridge of the hypoblast. In the succeeding stages the medullary groove becomes continued back to the opening of the passage, which then becomes enclosed in the medullary folds, and forms a true neurenteric passage. It becomes narrowed as the medullary folds finally unite to form the medullary canal, and eventually disappears.
1 Gasser, Der Primitivstreifen bei Vogelembryonen, Marburg, 1878. B. 42
650 EARLY DEVELOPMENT OF THE LACERTILIA.
I conclude this paper with a concise statement of what appears to me the probable nature of the much-disputed organ, the primitive streak, and of the arguments in support of my view.
In a paper on the primitive streak in the Qtiart. Journ. of Mic. Sci., in 1873 (p. 280) [This edition, p. 45], I made the following statement with reference to this subject : "It is clear, therefore, that the primitive groove must be the rudiment of some ancestral
feature It is just possible that it is the last trace of that
involution of the epiblast by which the hypoblast is formed in most of the lower animals."
At a later period, in July, 1876, after studying the development of Elasmobranch fishes, I enlarged the hypothesis in a review of the first part of Prof. Kolliker's Entwicklungsgeschichte. The following is the passage in which I speak of it 1 :
" In treating of the exact relation of the primitive groove to the formation of the embryo, Professor Kolliker gives it as his view that though the head of the embryo is formed independently of the primitive groove, and only secondarily unites with this, yet that the remainder of the body is without doubt derived from the primitive groove. With this conclusion we cannot agree, and the very descriptions of Professor Kolliker appear to us to demonstrate the untenable nature of his results. We believe that the front end of the primitive groove at first occupies the position eventually filled by about the third pair of protovertebrae, but that as the protovertebrae are successively formed, and the body of the embryo grows in length, the primitive groove is carried further and further back, so as always to be situated immediately behind the embryo. As Professor Kolliker himself has shewn it may still be seen in this position even later than the fortieth hour of incubation.
"Throughout the whole period of its existence it retains a character which at once distinguishes it in sections from the medullary groove.
" Beneath it the epiblast and mesoblast are always fused, though they are always separate elsewhere ; this fact, which was
1 Journal of Anat. and Phys., Vol. X. pp. 790 and 791. Compare also my Monograph, on Elasmobranch Fishes, note on p. 68 [This edition, p. 281].
EARLY DEVELOPMENT OF THE LACERTILIA. 6$ I
originally shewn by ourselves, has been very clearly brought out by Professor Kolliker's observations.
" The features of the primitive groove which throw special light on its meaning are the following :
"(i) It does not enter directly into the formation of the embryo.
" (2) The epiblast and mesoblast always become fused beneath it.
" (3) It is situated immediately behind the embryo.
" Professor Kolliker does not enter into any speculations as to the meaning of the primitive groove, but the above-mentioned facts appear to us clearly to prove that the primitive groove is a rudimentary structure, the origin of which can only be completely elucidated by a knowledge of the development of the Avian ancestors.
" In comparing the blastoderm of a bird with that of any anamniotic vertebrate, we are met at the threshold of our investigations by a remarkable difference between the two. Whereas in all the lower vertebrates the embryo is situated at the edge of the blastoderm, it is in birds and mammals situated in the centre. This difference of position at once suggests the view that the primitive groove may be in some way connected with the change of position in the blastoderm which the ancestors of birds must have undergone. If we carry our investigations amongst the lower vertebrates a little further, we find that the Elasmobranch embryo occupies at first the normal position at the edge of the blastoderm, but that in the course of development the blastoderm grows round the yolk far more slowly in the region of the embryo than elsewhere. Owing to this, the embryo becomes left in a bay, the two sides of which eventually meet and coalesce in a linear fashion immediately behind the embryo, thus removing the embryo from the edge of the blastoderm and forming behind it a linear streak not unlike the primitive streak. We would suggest the hypothesis that the primitive groove is a rudiment which gives the last indication of a change made by the Avian ancestors in their position in the blastoderm, like that made by Elasmobranch embryos when removed from the edge of the blastoderm and placed in a central situation similar to that of the embryo bird. On this hypothesis the
652 EARLY DEVELOPMENT OF THE LACERTILIA.
situation of the primitive groove immediately behind the embryo, as well as the fact of its not becoming converted into any embryonic organ would be explained. The central groove might probably also be viewed as the groove naturally left between the coalescing edges of the blastoderm.
"Would the fusion of epiblast and mesoblast also receive its explanation on this hypothesis ? We are of opinion that it would. At the edge of the blastoderm which represents the blastopore mouth of Amphioxus all the layers become fused together in the anamniotic vertebrates. So that if the primitive groove is in reality a rudiment of the coalesced edges of the blastoderm, we might naturally expect the layers to be fused there, and the difficulty presented by the present condition of the primitive groove would rather be that the hypoblast is not fused with the other layers than that the mesoblast is indissolubly united with the epiblast. The fact that the hypoblast is not fused with the other layers does not appear to us to be fatal to our hypothesis, and in Mammalia, where the primitive and medullary grooves present precisely the same relations as in birds, all three layers are, according to Hensen's account, fused together. This, however, is denied by Kolliker, who states that in Mammals, as in Birds, only the epiblast and mesoblast fuse together. Our hypothesis as to the origin of the primitive groove appears to explain in a fairly satisfactory manner all the peculiarities of this very enigmatical organ ; it also, relieves us from the necessity of accepting Professor Kolliker's explanation of the development of the mesoblast, though it does not, of course, render that explanation in any way untenable."
At a somewhat later period Rauber arrived at a more or less similar conclusion, which, however, he mixes up with a number of opinions from which I am compelled altogether to dissent 1 .
The general correctness of my view, as explained in my second quotation, appears to me completely established by Gasser's beautiful researches on the early development of the chick and goose 2 , and by my own observations just recorded on the lizard. While at the same time the parallel between the blastopore of Elasmobranchii and of the Sauropsida, is rendered
1 " Primitivrinne u. Urmund," Morphologisches Jahrbuch, Band II. p. 551.
2 Gasser, Der Primitivstreifen bei Vogelembryonen, Marburg, 1878.
EARLY DEVELOPMENT OF THE LACERTILIA. 653
more complete by the discovery of the neurenteric passage in the latter group, which was first of all made by Gasser.
The following paragraphs contain a detailed attempt to establish the above view by a careful comparison of the primitive streak and its adjuncts in the amniotic vertebrates with the blastopore in Elasmobranchii.
In Elasmobranchii the blastopore consists of the following parts: (i), a section at the end of the medullary plate, which becomes converted into the neurenteric canal 1 ; (2), a section forming what may be called the yolk blastopore, which eventually constitutes a linear streak connecting the embryo with the edge of the blastoderm (vide monograph on Elasmobranch fishes, pp. 281 and 296). In order to establish my hypothesis on the nature of the primitive streak, it is necessary to find the representatives of both these parts in the primitive streak of the amniotic vertebrates. The first section ought to appear as a passage from the neural to the enteric side of the blastoderm at the posterior end of the medullary plate. At its front edge the epiblast and hypoblast should be continuous, as they are at the hind end of the embryo in Elasmobranchii, and, finally, the passage should, on the closure of the medullary groove, become converted into the neurenteric canal. All these conditions are exactly fulfilled by the opening at the front end of the primitive streak of the lizard (vide woodcut, fig. I, p. 647). In the chick there is at first no such opening, but, as I hope to shew in a future paper, it is replaced by the epiblast and hypoblast falling into one another at the front end of the primitive streak. At a later period, as has been shewn by Gasser 2 , there is a distinct rudiment of the neurenteric canal in the chick, and a complete canal in the goose. Finally, in mammals, as has been shewn by Schaffer 3 for the guinea-pig, there is at the front end of the primitive streak a complete continuity between epiblast and hypoblast. The continuity of the epiblast and hypoblast at the hind end of the embryo in the bird and the mammal is a
1 I use this term for the canal connecting the neural and alimentary tract, which was first discovered by Kowalevsky.
2 Loc. cit.
3 " A contribution to the history of the development in the Guinea-pig," Journal of Anat. and Phys. Vol. xi. pp. 332 336.
654 EARLY DEVELOPMENT OF THE LACERTILIA.
rudiment of the continuity of these layers at the dorsal lip of the blastopore in Elasmobranchii, Amphibia, &c. The second section of the blastopore in Elasmobranchii or yolk blastopore is, I believe, partly represented by the primitive streak. The yolk blastopore in Elasmobranchii is the part of the blastopore belonging to the yolk sac as opposed to that belonging to the embryo, and it is clear that the primitive streak cannot correspond to the whole of this, since the primitive streak is far removed from the edge of the blastoderm long before the yolk is completely enclosed. Leaving this out of consideration the primitive streak, in order that the above comparison may hold good, should satisfy the following conditions :
1. It should connect the embryo with the edge of the blastoderm.
2. It should be constituted as if formed of the fused edges of the blastoderm.
3. The epiblast of it should eventually not form part of the medullary plate of the embryo, but be folded over on to the ventral side.
The first of these conditions is only partially fulfilled, but, considering the rudimentary condition of the whole structure, no great stress can, it seems to me, be laid on this fact.
The second condition seems to me very completely satisfied. Where the two edges of the blastoderm become united we should expect to find a complete fusion of the layers such as takes place in the primitive streak ; and the fact that in the primitive streak the hypoblast does not so distinctly coalesce with the mesoblast as the mesoblast with the epiblast cannot be urged as a serious argument against me.
The growth outwards of the mesoblast from the axis of the primitive streak is probably a remnant of the invagination of the hypoblast and mesoblast from the lip of the blastopore in Amphibia, &c.
The groove in the primitive streak may with great plausibility be regarded as the indication of a depression which would naturally be found along the line where the thickened edges of the blastoderm became united.
With reference to the third condition, I will make the following observations. The neurenteric canal, as it is placed at the
EARLY DEVELOPMENT OF THE LACERTILIA.. 655
extreme end of the embryo, must necessarily, with reference to the embryo, be the hindermost section of the blastopore, and therefore the part of the blastopore apparently behind this can only be so owing to the embryo not being folded off from the yolk sac ; and as the yolk sac is in reality a specialised part of the ventral wall of the body, the yolk blastopore must also be situated on the ventral side of the embryo.
Kolliker and other distinguished embryologists have believed that the epiblast of the whole of the primitive streak became part of the neural plate. If this view were correct, which is accepted even by Rauber, the hypothesis I am attempting to establish would fall to the ground. I have, however, no doubt that these embryologists are mistaken. The very careful observations of Gasser shew that the part of the primitive streak adjoining the embryo becomes converted into the tail-swelling, and that the posterior part is folded in on the ventral side of the embryo, and, losing its characteristic structure, forms part of the ventral wall of the body. On this point my own observations confirm those of Gasser. In the lizard the early appearance of the neurenteric canal at the front end of the primitive streak clearly shews that here also the primitive streak can take no share in forming the neural plate.
The above considerations appear to me sufficient to establish my hypothesis with reference to the nature of the primitive streak, which has the merit of explaining, not only the structural peculiarities of the primitive streak, but also the otherwise inexplicable position of the embryo of the amniotic vertebrates in the centre of the blastoderm.
656 EARLY DEVELOPMENT OF THE LACERTILIA.
^ DESCRIPTION OF PLATE 29.
COMPLETE LIST OF REFERENCE LETTERS.
am. Amnion. ch. Notochord. ck '. Notochordal thickening of hypoblast. ep, Epiblast. hy. Hypoblast. m.g. Medullary groove, me.p. Mesoblastic plate. ne, Neurenteric canal (blastopore). pr. Primitive streak.
SERIES A. Sections through an embryo shortly after the formation of the medullary groove. X I2O 1 .
Fig. i. Section through the trunk of the embryo. Figs. 2 5. Sections through the neurenteric canal.
Fig. B. Surface view of a somewhat older embryo than that from which Series A is. taken, x 30.
SERIES B. Sections through the embryo represented in Fig. B. x 120.
Fig. i . Section through the trunk of the embryo.
Figs. 2, 3. Sections through the hind end of the medullary groove.
Fig. 4. Section through the neurenteric canal.
Fig. 5. Section through the primitive streak.
Fig. C. Surface view of a somewhat older embryo than that represented in Fig. B. x 30.
1 The spaces between the layers in these sections are due to the action of the hardening re-agent.