Blastopore s Mesoderm and Iffetamerie Segmentation.
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1 BLASTOPOEB, MBSOBEEM AND METAMESIO SEGMENTATION. 15 Blastopore s Mesoderm and Iffetamerie Segmentation. By W. M. Caldwell;, H.A., fellow of Caius College, and Balfour Studeat in the University of Cambridge. With Plate II. A TEAK ago my observations on the development of certain, forms of invertebrate animals suggested an explanation, of tie behaviour of the blastopore, and led me to consider the various speculations concerning the middle germinal layer put forward in recent years. The theory which I thus deduced embraces the question of metameric segmentation. On my voyage to Australia I wrote the present paper. Meanwhile my friend Mr. Sedgwiek, to whom I had written some of my conclusions, was preparing a contribution to the same subject. Since then Mr. Sedgwick's paper 1 has appeared, and I find not only that my conclusions as to the meaning of segmentation are fundamentally different; but also that he leaves the larger question of mesoderm untouched. The origin of mesoderm in Phoronis was the startingpoint of my inquiry. I shall first describe the facts in this animal, and I would point out that my discoveries are due entirely to the facilities for investigating minute embryos afforded by my method of obtaining automatic series of sections. I failed to observe the details which are contained in the present paper in my original sections from which a preliminary account {' Proc. Eoy. Soc.' 1882) was composed.! ' Quart. Journ. Mic. Soi.,' 1884, " Origin of Metameric Segmentation."
2 16 W. H. CA1DWELL. DEVELOPMENT OF PHOKONIS. The details of the segmentation of the ovum are not required in this paper. A planula slightly oval in form is the final term of the process. The long axis of this planula coincides with the future long axis of the gastrula. One half of the cells are large (endoblast), the other half are small (ectoblast). GASTRULATION. The gastrula is formed by invagination. The first sign of this is the flattening of the endoblast-half of the oval planula. The sides begin to grow over the endoblast, and this takes place in such a way that the saucer-shaped structure is deepened towards the future anterior end (PL II, fig. 1). The anterior end also grows rapidly over the endoblast, thus early indicating the future prseoral lobe. The bilateral symmetry is thus clearly marked. Posteriorly the sides fold over so as to meet in the middle line (PI. II, fig. 9). The cavity of the archenteron is now sufficiently large to form lips to the blastopore. Quite posteriorly the lips completely fuse, so that during the gastrulation the extreme posterior portion of the archenteric cavity is obliterated (PI. II, fig. 10). It is represented by a fused solid mass of cells (/ _). The lips of the blastopore continue to approach the middle line, and as they touch fuse with each other. This fusing proceeds from behind forwards. The blastopore has in this way become divided into two parts exactly comparable to the parts long known in some vertebrates (PI. II, fig. 2). I shall speak therefore of the posterior portion as the primitive streak, and the groove along the line of closure as the primitive groove. The invagination has now produced a gastrula with an opening situated in the anterior portion of the blastopore into a large archenteric cavity (PL I, fig. 11). I shall now use the terms dorsal and ventral as defined by the non-blastoporic and the blastoporic regions respectively. The ventral surface now begins to grow very much more rapidly than the dorsal. The growth results in the posterior point of the primitive streak becoming terminal. The exact* behaviour of
3 BLASTOPOEE, MESODERM AND METAMEEIC SEGMENTATION. I? the cells of the middle of the primitive streat is as follows. About the middle of the primitive streak the ectoblastic elements divide very rapidly, and very soon the primitive groove disappears in this region (si. PL II,figs. 2 6). Coincidently with this a space appears between ecto- and endoblast (PL II, fig. 18, v). Consider the fate of a single one of the cells of the primitive streak. This ceil is destined to give rise by division to both ecto- and endoblast. The ectoblastic portion increases more rapidly than the endobiastic, and soon the latter is no longer in contact with the former, i.e. a space has arisen in the median ventral line. This space extends both anteriorly and posteriorly. The primitive groove BOW only remains as a pit at the posterior end of the embryo (fig. 4, g). The anterior opening of the blastopore remains open and becomes the month of the future Phoronis, the posterior pit is destined to undergo some very remarkable changes which will be described below. During these changes the original solid mass of cells the posterior portion of the primitive streak remains unaltered as a cord connecting the archenteron with the ectoderm. THE SEPARATION OF THE MESOBLAST. Previous Observations. Kowalewsky originally described the mesoblast as originating in Phoronis by delamination from the ectoderm (vide Plate II, fig. 13). This mistake arose from the ectoderm cells being darker at their base. Recently Metschnikoff and Foettinger have attempted to solve the problem of mesoderm formation. While they have both recognised Kowalewsky's error, they have fallen into other mistakes. Metschnikoff describes some mesoblastie cells already present in the blastula stage; hefiguresfour of them in Ms fig. 30. In each cell Metschnikoff has drawn a nucleus. I have frequently observed this appearance of cells. It is caused, however, by the amoeboid processes of the endoderm ceils growi% into the segmentation cavity. This is easily proved by making real sections. Another possible explanation of Metschnikoff's account may lie in the presence of certain peculiar bodies in VOL. XXV. NEW SEE. B
4 18 W. H. CALDWELL. the early gastrula stages. In the endoderm. cells little spherical masses of apparently the same material as the body of the cells themselves are frequently found. Each little mass in hardened embryos is separated off by a clear space. I have traced these bodies from their birthplace into the body cavity. They never possess a nucleus, and they disappear at a very early age. Their significance remains unknown to me unless they be merely an excess supply of nutriment analogous to food yolk. Foettinger has arrived at somewhat extraordinary results. He says, " J'ai non seulement constate 1'existence des premiers elements-mesodermiques a des stades plus jeunes que celui signale par Metschnikoff, mais encore je crois pouvoir reculer leur premiere apparition jusqu'a Fceuf en voie de segmentation." The bodies referred to the mesobiast are, I believe, either due to the reagents used in preparing the embryos, or are the bodies referred to above. I have observed them frequently, but it is certain that they have nothing to do with the true mesobiast, whose origin I shall now describe. Before the lips of the blastopore meet there is no mesobiast (fig. I). When the closing of the blastopore has already extended sufficiently far forwards to shut off a small archenteric cavity, two pouchings of the endoderm occur on either side of the blastopore (fig. 8, ad). Each pouch is longitudinally extended in the direction of the long axis of the body, and is deeper towards its anterior end. The endoderm cells covering the region of the pouch now undergo some division (fig. 8), and a mass of cells is budded off on either side {me'). These cells as they are formed arrange themselves into a sac enclosing a cavity (fig. 17, ad). These cavities, however, never communicate with the cavity of the gut. The pouch of the endoderm is soon obliterated, and the cells return to the size of the other endoderm cells. The hind part of each pouch lies about opposite to the most anterior point where the lips of the blastopore have closed. On either side of the primitive streak a few mesobiast cells are budded off from the cells forming the primitive streak (fig. 18, me"). Behind the primitive groove becomes deeper, and
5 BLASTOPOKE, MESODEEM AND META3TERIC SEGMENTATION. 19 this deepening continues after the middle part is obliterated (figs. 4, 6, 11, and 12). The deepening of the groove soon forms a very definite pit {g). This pit, when by the growth of the ventral surface it has become nearly terminal,, grows into two pouches which project into the cayity between the skin and gut on either side of the solid cord of cells, which is the persistent hind part of the original primitive sheath (fig. 13 and fig. 14, pd). These pouches are derived from cells homologous with those which have already given rise to mesoblast. The continuity of this posterior pair of pits with the anterior is kept up by the few cells (me") budded off in the middle of the primitite streak. The same growth which opened up the space between ectoblast and endoblast has separated the anterior and posterior mesoderm. The fact that in Phoronis the two ends of each mesodermie pouch are actually connected by an intermediate cord of cells depends on this formation of a primitive streak along the whole line of closure of the blastopore. NEPHEIDIA. The posterior pair of mesodermie diverticnla open in the middle line to the exterior. The closure of this opening proceeds in such a way that each pouch remains open to the exterior by a small pore on either side of the middle line. I believe though this fact is not established so certainly as those above concerning the mesoderm that each pore persists as the opening of the nephridium of its own side. The nepitridia appear eoincidently with the final narrowing of the mesodermic pores, but I have yet no sections showing the cells in the neighbourhood of the pores taking on the form of the Intracellularly perforate excretory cells. The formation of these excretory cells, which lie in a blood space of the splanchnopleure and not in the body cavity, I have independently traced from the mesodennic cells of the posterior pouches.
6 20 W. H. OALDWELL. ANUS. Meanwhile the remnant of the primitive streak, the posterior solid cord of cells, opens up, and forms a canal leading from the archenteron to the exterior (fig. 15). The alimentarycanal is now complete, mouth and anus having been derived from the blastopore (fig. 7, m and a). HYPOTHESIS. With the help of the various morphological laws implied by such terms as precocious segregation, superlarvation, abbreviation, &e., it is possible to solve almost any morphological problem in several ways all equally probable. The speculations which follow, I am induced to add to those already existing, not from any belief in their absolute value, but because they go in the direction of simplification. The theory which I am about to state reduces the various origins of the mouth and anus to one type. The same hypothesis gives an explanation of the various modes of origin of the mesoderin, and leads to a view of the meaning of metamerie segmentation which, so far as I knowj has not been hitherto suggested. Given a gastrsea already become bilaterally symmetrical by the elongation of the blastopore and the differentiation of anterior inhalent and posterior exhalent currents, and in which the main development of organs takes place around the mouth, so that the mesoderm thus resulting comes to lie in development as two masses of cells on either side of the body. 1 I propose to show that the elongation of a long axis of the body is a possible cause of I. The obliteration of the relation of blastopore to mouth and anus. II. The masking of the original mode of mesodermic formation. III. Metamerie segmentation. 1 Whether the mesoderm originally arose as diverticuia or not does not concern the present speculation.
7 BLASTOPORE, MESODERM AND METAMERIC SEGMENTATION. 21 I. The Obliteration of the Relation of Blastopore to Mouth and Anns. Previous Observations. Since the time of the Gastraea Theory many writers have occupied themselves with the blastopore. Lankester (This Journal, 1877), in accordance with, his planular theory, came to the conclusion, that the coincidence of mouth and aaus with the blastopore was only a developmental convenience. He says (loc.cit.), "Regarding, as I do, the blastopore as an orifice of a secondary nature, esisting solely in relation to the invagination process, and originating after mouth and anus had made their appearance in the progress of animal evolution, I seek to explain its occasional relation to the mouth and to the anus as cases of adaptation." Balfour, after enumerating the different fates of the "blastopore in the animal kingdom, says, " 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 number of groups in which a slit-like blastopore has been described is very considerable (vide Balfour, vol ii, p. 282). Lankester was the first to suggest that a slit-like blastopore which might close at either end would, if taken as the ancestral type, account for the various fates of the blastopore in molluscs. Hatschek, in his paper on Teredo, has suggested the possibility of phylogenetically deriving the anus which arises in this animal; secondarily, as an ectodermic invagination from part of a slit-like blastopore. But he bases this view on the fact that the anus corresponds in position with the hind wall of the. gastrula mouth. Metschnikoff, in combating Hatsehek's views on the early expression of bilateral symmetry, has denied the ancestral character of the slit-like blastopore. He says, " Kaiin man dem gesehlitzten grossen Biastopor keine paiingenetisehe Bedeutung zuschreiben und muss ihn als eine embiyonale Anpassungs-erschehrangansehen." Sedgwick (loc. cit.,p. 27) concludes that " the mouth and anus of the Triploblastica are
8 22 W. H. CALDWELL. derived from the primitive mouth." I fail to see how his theory on p. 34 explains the behaviour of the blastopore. In the first place his conception of the blastopore is diiferent from that used in the present paper. Page 35 he writes, " Consequently the only course open is that the mouth should be formed as a secondary perforation entirely independent of the blastopore." Sedgwick's theory is contained in the following passages (p. 34): " My view is that in those animals in which it does not give rise to the mouth and anus, it functioned as the larval mouth while the animal was developing, and persisted until parts of the embryo were developed between it and the position of the mouth and anus of the adult, which parts had arisen in the phylogenetic history in the adult after the primitive mouth had completely divided into the mouth and anus. These parts never had. been traversed by the original slit-like mouth, because they had. appeared at a stage in evolution subsequent to the stage in which the mouth and anus were one. It cannot therefore be a matter of surprise if the blastopore does not elongate and bisect these latter structures, which never had in the history of the animal been perforated by the blastopore." I ask, how have the cells which are to form mouth and anus anything to do with blastopore? My hypothesis is as follows. 1 The behaviour of the blastopore in Phoronis is obviously due to the attainment of a terminal anus. Suppose the long axis of the body to increase still more rapidly while the posterior part of the blastopore still remains terminal. Suppose in the early stages of development the importance of a complete alimentary canal is not equal to the importance of the body form, then the tendency of the endoblast to divide into anterior and posterior portions attached to anterior and posterior parts of the blastopore respectively might be consummated. The behaviour of the cells in the middle of the primitive streak of Phoronis, which resulted in the opening of a space between endoderm and ectoderm, would tend to begin at an earlier stage. 1 Delamination need not be discussed, since the existing hypotheses (vide Balfour, 'Embryology,' vol. ii) are sufficient to bring the case under my theory.
9 BtASTOPOBE, MESODEEM AXD METAMEEIC SEGMENTATION. 23 What would be the structure of a pianula when this influence has reached Tback to the preinvaginated stages? The ectoderm cells would grow in from either side, and encroach on the solid mass of endoblast until this (i. e. endoblast) would be completely divided into anterior and posterior masses. The endoblast may be divided in this way into any number of separate portions (ef. below metameric segmentations). Let invagination now take place; each mass of endoblast will be invaginated. The invaginated endoblast will grow according as it has been divided into endoderm or mesoderm; such division may have taken place in a great many ways (vide mesoderm below); when the anterior endoblastie mass is the larger we have a so-called oral blastopore, e. g. Pilidiuin, Phascolosoma, and Phoironis, according to previous observers; when the posterior is the larger we have an anal blastopore, e. g. Paludina, Serpula, and Echinodermata. Let the invagination of the different endoblastie masses cease to be synchronous, and the primitive relations will become still more marked. The extreme cases are described as stomodosa and proctodcea. The difference between Sedgwiefs view and my own consists in the fact that I suppose that portions of the biastopore actually exist beyond the " parts which, in the phylogenetic history in the adult, had arisen after the primitive mouth had completely divided into the mouth and anus." II. The Masking of the Original Mode of the Origin of Mesodermic Formation. In Phoronis the original pair of diverticula are almost divided into two pairs. The anterior pair produce only a small proportion of the future mesodermic structures. Argiope is an instance of the anterior mesoderm being large. No posterior mesoblast has yet been described in this form. The mesenehyme of the preoral lobe of the Hertwigs is the same anterior mesodermic diverticula reduced in the oppositedirection. In Phoironis the anterior mesoderm would be described as of endoblastie origin, the middle as originating at the lips of the blastopore, while the posterior pouches would be assigned to the ectoblast. But the connec-
10 24 W. H. CALDWELL. tion between these three methods, though obvious in Phoronis, has not been explained in the same way in the rest of the Triploblastica. The six diagrams (fig. 19) represent six different modes of formation; they may all coexist in the same animal. Thus, in Phoronis we find those represented in the diagram by 3, 4, and 6, and in the Chick and other Vertebrates 4 and 6. III. Metameric Segmentation. In Phoronis the elongation of the blastopore produces two pairs of masses of mesoblast, each of which might be regarded as constituting a " mesodermic somite;" but in Phoronis the first long axis developed is not to be the long axis of the adult. The long axis of an adult Phoronis is exactly at right angles to that of the larva. The further slight extension of the larval long axis is thus able to proceed pari passu with the growth of the posterior pair of mesodermic pouches. In Chaetopoda, Arthropoda, and Vertebrata the long axes of adult and larva are identical. The elongation of the body in these forms takes place before the mesoderm grows. The same cause which separated the mesoderm in Phoronis operates during a much longer developmental period. The mesoderm cannot keep pace with the ectoderm. It must therefore be left to afterwards complete its growth. The various positions in which it may remain give rise to the various origins of the mesoderm. Take Amphioxus, where the mesoderm has remained entirely in the endoblast. Here we have a regular elongation of the body taking place when the mesodermic cells are still undifferentiated. The mesodermic diverticula are regularly drawn out, and as regularly they leave small portions of the whole in front. Hatschek has described a shallow groove connecting the separated diverticula on each side, which is explained by the present hypothesis. I take it to be of the same nature as the connecting strand of mesoderm in Phoronis. Echiurus (Hatschek) is a form where the greater part of the mesoderm remains near the posterior pole of the long axis as in Phoronis. As the long axis grows the mesoblast has to be left
11 BLASTOPOEE, MESODEEM AND METAMERfC SEGMENTATION. 25 in formative masses, which afterwards grow to line the body cayity (in Echiurus, however, the mesoderm much more nearly keeps pace with the eetoderm than in Amphioxus). Thus, I consider that in Cfaaetopoda, Arthropoda, and Vertebrata the mesoderm will tend to be left in regular pairs of masses, while the elongation of the body is taking place; I seek to explain the whole of the facts of metameric segmentation as arising from the necessities of development. In Phoronis the external openings of the nephridia are parts of the blastopore. The same considerations which have been applied to the mouth and anus, mesoderm and metameric segmentation bear on the question of the origin of nephridia. The nephridial portions of the mesoderm may remain in various positions, in other words, the nephridia may in accordance with my hypothesis arise as single or as serial ectoblastic or endoblastic pairs of pouches with or without connecting longitudinal canals or cords. Instances of most of these possible modes of origin have been described in the different groups of animals. The bearing of the above facts and hypotheses on the nervous system, gillslits, notochord, and other organs, will be obvious to anyone who has followed me so far. I hope to be excused from entering into completer discussion of my hypothesis by reason of the want of books of reference in my present situation out of the world. SUMMARY. Facts in the development of Phoronis 1. The blastopore gives rise to both mouth and anus. 2. The mesoderm arises in an anterior pair of endobiastie modified diverticula, and in a posterior pair of eetoblastic diverticula connected by a few mesodermic cells derived from the middle of a primitive streak. 3. The nephridial openings to the exterior are parts of the blastopore. Preliminary interpretation suggested by these facts of the development of Phoronis
12 26 W. H. OALDWELL. 1. A gastraea with slit-like mouth and a pair of lateral diverticula giving rise to mesoderm was the ancestor of Phoronis. 2. The rapid growth of ectoderm in the median ventral line nearly succeeded in destroying the continuity of the primitive streak. 3. The necessity of an early attainment of a terminal position by the anus caused the ectoderm to grow more rapidly than, the endoblast, and resulted in a division of the mesoderm into anterior and posterior parts. 4. The nephridia, which might have remained either wholly or in part with the anterior, have attached themselves entirely to the posterior mesoderm. Extension of this interpretation to the other Tripleblastiea 1. Phoronis is the first step towards a complete division of the blastopore. The inducing cause of such division is the elongation, of the body, while the endoblast is still in an embryonic condition. 2. The division of blastopore caused the division of mesoderm. 3. The division of mesoderm results in i. The masking of the original mode of mesoderm formation. ii. Metameric segmentation. IN CAMP, BUENEII RIVER, QUEENSLAND ; July 27,1884.
13 BLASTOPOE-E, MESODEBM AND JTETAMEEIC SEGMENTATION. 27 EXPLANATION OF PLATE II, Illustrating Mr. "W. H. Caldwell's paper on " Blastopore, Mesoderm and Metameric Segmentation." List of Reference Letter*. Blastopore, LI. Mouth, «. Anus, a. Primitive streak, p. s. Primitive groove, p. g. Posterior pit, g. Posterior solid cord. r. Anterior mesodermic diverticulum, a. d. Posterior mesodemic divertigniiiin, p. d. Mesoderm, me. Praoral lobe, p.!. Arehenteron, ar. External opening of nepliridium, s. Body cavity (coelom), a. Splancbnopleuric vascular space, v. Nutritive (?) body, x. All the fignres, both of whole embryos and of sections, were drawn, by means of Zeiss's two-prism camera, from permanent preparations in Canada balsam. The embryos were treated as follows: Mixture of two relumes corrosive sublimate -f- one vol. glacial acetic acid for 1 second, water 15 seconds, alcohol, 50 per cent., 3 minutes, alcohol 70 per cent. Eigs Zeiss's oe. 2, obj. D. Eigs Zeiss's oc. 2, obj. l-12th komog. imm. All the embryos beloag to the species of Phoroms, lifing in the harbour of Naples in dense colonies without sand adhering to their tubes, except that of which Fig. 13 is a section. This is aa Australian PhoroniSj discovered in Port JacksoE by Mr. Haswell, of Sydney Uni?ersity. The sections drawn are taken from complete series. Each sectioe is '005 mm. thick. I have series '0025 mm. thick. These, thongh necessary for observation, purposes, are not so convenient for drawing. FIGS Eour embryos, showing mode of closure of the blastopore. Eg. 1. Blastopore, 61., before meeting of lips. Fig. 2. Blastopore fused posteriorly: opes part=mouth, m.; dosed part= primitive streak aad groove, p. g. Fig. 3. Primitive groove, p.g.\ disappearing praorai lobe, p. I. Kg. i. Primitive groove enlarging into pit, g., posteriorly; prseorai lobe, p. I. EIGS. 5 aad 6. Two embryos viewed from the left side. Braeorai lobe, p. I.; primitive groove, p. g.; mouth, m.; posterior pit, g. Fig. 7. Older embryo with, complete alimentary canal. Month, m.; anas, a.; external opening of nephridium, «. FIGS Three sections in a nearly transverse plane of an embryo in a stage betweea that of Fig. 1 and that of Fig. 2.
14 28 W. H. CA.LDWELL. Fig. 8. In front of mouth. Anterior mesodermie diverticula, a. d.; anterior mesodermic cell, me.; arehenfceron, ar. Fig. 9. Through the fusing lips of the blastopore. Primitive streak, p. s.; archenteron, ar. Fig. 10. Through the posterior part of the primitive streak. Primitive groove, p.g.\ posterior solid cord of cells, r. FIG. 11. Median section, longitudinal vertical, through a slightly older embryo than Figs. 8, 9, and 10. Pneoral lobe, p. 1.; anterior mesoderm, me'.; mouth, m.; archenteron, ar.; posterior pit, g ; posterior solid cord of cells, r; Nutritive (?) body, x; body cavity, c. FIG. 12. Embryo slightly older than Fig. ±. Median longitudinal vertical section. Prsaoral lobe, p. I.; anterior mesoderm, m'.; body cavity, c.; vascular space, v.; middle mesoderm, m".; posterior mesoderm, rd".; archenteron, ar.; posterior pit, g; Mouth, m. FIG. 13. Embryo, Australian species, nearly same stage as Fig. 12. Longitudinal horizontal section. Archenteron, ar.; anterior mesoderm, me'; posterior mesodermic diverticula, p. d.; posterior pit, g. FIG. 14. Nearly same section as Fig. 13. Vascular space, v.; posterior pit, g; archenteron, ar.; anterior mesoderm, me".; posterior diverticula, p. d.; posterior mesoderm, me'". FIG. 15. Embryo, same stage as Fig. 12. Longitudinal horizontal section. Reopening of posterior cord of cells to form rectum and anus, a.; anterior mesoderm, me'.; archenteron, ar. FIG. 16. Embryo, same stage as Fig. 12. Transverse section through posterior diverticula, p. d.; posterior mesoderm me"'.; arehenteron, ar. FIGS. 17 and 18. Embryos about the stage of Fig. 3. Two transverse sections. Anterior diverticula, a. d.; body cavity, c.; vascular space,».; primitive streak, p. s.; primitive groove, p. g.; middle mesoderm, me".; archenteron, ar.; nutritive (?) body, x. FIG. 19. Six diagrams, illustrating the typical modes of mesoderm formation, e. g. 1. Peripatus, cf. Hertwig's " Coslom-theorie," PI. ii, fig. of insect embryo. 2. Amphioxus. 3. Nemertine larva of Desor (?), Phoronis (posterior). 4. Pristiurus, Phoronis (anterior). 5. Lopadorhynchus (Kleinenberg). 6. Primitive streak region, many Vertebrates and Phoronis.
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