The Origin and Significance of the Metamorphosis of Actinotrocha

It may be convenient to preface the following description, with a short summary of the more important points. The larva has a somewhat elongated body with a series of long ciliated arms nearly encircling the body behind the mouth, and a narrow belt of long cilia just anterior to the anus, which is situated at the posterior end of the body. The mouth is on the ventral side near the anterior end, and is overarched by a very large hood-like expansion of the body wall, the præoral lobe. The hood is richly ciliated and serves to produce currents of water flowing towards the mouth, which bring with them particles of food.

The only internal organ at first is the digestive canal, consisting of a distinct oesophagus, a capacious stomach, and a longer or shorter intestine. In time, however, the ventral wall of the body thickens at a point in the middle line just behind the circlet of the arms. This thickening is apparently produced by an infolding of the body wall; at any rate, it soon becomes hollow and pouch-like, and communicates with the exterior by means of a small opening, while fibrous or muscular connections between it and the stomach walls may be observed. The pouch grows rapidly, and at length comes to occupy a large part of the perivisceral cavity, doubling back and forth, and becoming transversely folded on its inner wall.

When the pouch has attained its complete development the larva becomes sluggish, sinks to the bottom, and the body usually contracts forcibly, so that it becomes shortened and rounded, and the walls become tense from the internal pressure thus produced. Suddenly, at what Metschnikoff appropriately terms the “critical stage” of the metamorphosis, the pouch turns itself outward through its external opening, unrolling like the finger of a glove or the eye tentacle of a snail. As it unrolls, the middle part of the digestive canal is drawn out into its cavity, thus forming a long U-shaped loop. At the same time the larval body shrinks together, and is doubled up toward the dorsal side, so that the mouth and anus are brought close together. The hood is withdrawn into the oesophagus, leaving only a small remnant, which overhangs the mouth and persists as an epistome. The greater part of each swimming arm undergoes a kind of granular disintegration and drops off, leaving only a small thickened basal portion, which becomes directed forwards, and subsequently grows into the corresponding tentacle of the adult Phoronis. The larval body fuses completely with the everted pouch, which now constitutes the greater part of the body of the worm. The subsequent external changes consist merely in the elongation of the tentacles and a great increase in their number, and the elongation of the body. The worm secretes for itself a membranous tube, in which it dwells, protruding only the extremity with its crown of tentacles. The resemblance of the latter to the lophophore of a hippocrepian Polyzoön is wonderfully close, though this resemblance is undoubtedly adaptive and secondary. A clear idea of the metamorphosis may be gained from the diagrammatic figs. 15 to 19.

Figure 1 represents a lateral view of the first stage figured by Metschnikoff. At h. is the hood; m. is the mouth leading by a short oesophagus to the stomach (st.). The latter communicates by a short intestine with the anus (a). Rudiments of two swimming arms are seen at a’, a.” Fig. 2 gives a ventral view of the same; rudiments of the second pair of arms are seen at a”, a”. Fig. 3 is a corresponding view of a somewhat later stage with the first four arms now plainly indicated. The body is everywhere richly ciliated and the cilia are distinctly longer along the margin of the hood and at the tips of the arms. Fig. 4 represents a side view of a considerably later stage, with five pairs of well-developed, though still short, arms. A number of large black pigment spots have appeared. Neither the præ-anal belt of cilia, nor the ventral pouch, have yet been developed. These four figures are copied from Metschnikoff.

The following figures represent different stages in the development of the two Chesapeake species, which for convenience sake may be designated A and B. The two species have well-marked specific differences, but their metamorphoses are almost identical, and agree in the main with that of the form studied by Metschnikoff. A is characterised by a very short intestine and a correspondingly stout body, and shows a considerable resemblance to the form studied by Metschnikoff (figs. 5, 7, 11). B has a long slender intestine, and the posterior part of the body is correspondingly elongated. At the upper lateral portions of the stomach are two rounded glandular lobes, one on either side of the oesophagus. The hood, in the later stages at any rate, has a prominent conical ciliated elevation on the median line in front. This form is apparently identical with Actinotrocha branckiata, the species originally discovered by Johannes Müller.

Figure 5 represents form A shortly after the appearance of the pouch which is seen in optical section at p on the ventral side. The arms are sixteen in number; they diminish regularly in length toward the dorsal side, thus indicating the order in which they have appeared. On the extreme dorsal side the series is interrupted by a considerable interval. The arms are nearly solid, but contain narrow central channels, which are diverticula from the perivisceral cavity. There are a number of pigment spots irregularly scattered over the body. The præ-anal belt of cilia (a. r.) has appeared, the dorsal vessel is seen at v., and an accumulation of pseud-hæmal corpuscles has appeared at cor. on the wall of the stomach. By flattening out the creature under a compressor the opening into the pouch becomes apparent (fig. 7).

Figure 6 represents the corresponding stage of the other species as seen from the opposite side, showing the pouch (p.) lying in the perivisceral cavity between the stomach and the body wall. It shows the ventral pseud-hæmal vessel with, rudiments of the contractile cæca (c) which are so striking a peculiarity of the adult circulatory apparatus.

Figure 8 represents a considerably later stage, in which is shown a great advance in the development of the pouch. Bending at first toward one side of the body it folds upon itself, and returns to the opposite side, then turns sharply downward along the intestine, and finally bends upward again near its extremity. Its inner walls are transversely folded. The arms have increased to the number of twenty, and are thickened on the lower side just at the base, to form the first rudiments of the permanent tentacles. There are four masses of pseud-hæmal corpuscles, two lying at each side of the stomach.

Figure 9 gives a dorsal view of the same stage, to show the arrangement of the arms on the dorsal side. The folds of the pouch have here a somewhat different arrangement, and cannot be clearly followed. The rudiments of the tentacles are shown at p. a., and the broad contractile dorsal vessel at v.

Figure 10 represents a full-grown larva of B immediately before its metamorphosis. The folds of the pouch are voluminous, and occupy a large part of the perivisceral cavity; they have nearly the same disposition as in fig. 8. The tentacular rudiments are very distinct, and have become partly independent of the larval arms. Both dorsal and ventral pseud-hæmal vessels are well developed and, like the-cæcal appendages, are actively contractile. The masses of corpuscles (cor.) are large and very conspicuous from their red colour. Form A agrees essentially with B at this stage, though the body is much stouter, and the rudiments of the tentacles are much smaller and more closely united to the larval arms. ‘

The two species differ slightly as to the manner in which the metamorphosis is effected. In the case of A the larva sinks to the bottom, contracts very strongly, and the evagination of the pouch occupies but a few minutes. The process occupies in the case of B a much longer time, and the body is only slightly or, at first, not at all contracted.

Figure 11 represents the latter species at the critical stage, with the pouch about half unrolled. The inner extremity of the latter still extends to the back of the stomach. At b, b, are seen some of the fibrous connections between the intestinal walls and those of the pouch.

Figure 12 represents the creature with the pouch (the whole of which is not shown) wholly unrolled. The hood has been withdrawn into the oesophagus, the larval arms have dropped off, and the short tentacles are directed straight forwards, and form a circlet surrounding the mouth. The posterior portion of the larval body (p.), with the anus at its extremity (a.), is still distinct, and is bent at right angles to the long axis of the pouch, which must now be called the body proper. In time it becomes bent still further upwards, and, at the same time, is gradually withdrawn into and fuses with the remainder of the body. Ultimately it quite disappears, and the anus remains as an opening on the side of the body, immediately behind the circlet of tentacles.

Figure 13 represents A about twenty-four hours after the metamorphosis, when the larval body has completely fused with that of the adult. The body is soft and extensible, and, though it has numerous transverse folds when contracted, there is no indication of metamerism. The aboral extremity is extremely changeable in shape; two forms commonly assumed are shown. The surface is everywhere finely granular, and becomes distinctly tuberculose towards the aboral extremity.

New tentacles are henceforward constantly budded forth at the dorsal side of the lophophore, at about the rate of a new pair every day, until their number becomes a hundred or more, and they increase gradually in length.

Figure 14 represents the same individual as that shown in fig. 13 twenty-two days after metamorphosis, and practically in the adult condition. The tentacles are richly ciliated, and have exactly the same appearance and perform the same movements as in the Polyzoa. Each has, however, a cæcal vessel from the pseud-hæmal circumoral ring, and performs a distinctly respiratory function. The pseud-hæmal fluid is very remarkable from the presence of numerous large, oval, nucleated corpuscles, which look not very unlike the red corpuscles of frogs’ blood, though of less regular shape. They are also red in colour, and render all the branches of the pseud-hæmal system very conspicuous, so that their arrangement may be very easily made out. Jn neither of the Chesapeake species is there a vessel running along the intestine towards the anus, although such a vessel is figured by Metschnikoff. Nor can I agree with this observer that the corpuscles of the pseud-hæmal fluid are developed free in the perivisceral cavity to be drawn into the pseud-hæmal vessels at the time of metamorphosis. There cannot be the least doubt that in both our species these corpuscles are developed in solid masses adhering to the stomach walls, near the base of the tentacles, and I believe them to a rise within the cavity of a sinus, which becomes the circumoral ring of the adult. They never float freely in the perivisceral cavity, and cannot for a moment be confounded with the true blood-corpuscles of this cavity. During the metamorphosis these masses suddenly break up, and the corpuscles are almost immediately carried along within the vessels by the peristaltic contractions of the latter. During the later larval stages they are sometimes elongated towards each other, and connected by a narrow band containing a few corpuscles (see fig. 10); and repeated observations of the metamorphosis has convinced me that, for our species at least, Metschnikoff’s account is incorrect. Owing to the failure of attempts to make satisfactory sections of the larvæ I have been unable absolutely to demonstrate this point, which is of considerable importance from its bearings on the relation between the pseud-hæmal system and the body cavity.

Before advancing speculations as to the origin and significance of this most remarkable course of development, it is necessary to dwell for a moment on the systematic relations of Phoronis, and on certain structural features of the group to which it belongs. It is pretty well agreed that Phoronis is a Gephyrean, although a greatly modified and specialised representative of this peculiar group. Although the peculiarities of its development are so great as to lead so high an authority as Mr. Balfour to question the correctness of this identification, I believe, nevertheless, that these doubts are not well-founded. In all essential anatomical characters, so far as they are known, Phoronis agrees closely with such forms as Sipunculus or Phascolosoma. Its most striking characters, such, for example, as the close proximity of the mouth and anus and the high development of the oral tentacles, are simply exaggerations of characters possessed by the last-named genera. Almost all of the adult characters are readily explicable as the result of extreme adaptation to a strictly tubicolous life. In regard to the development, I shall endeavour to show that its peculiarities are almost certainly due to secondary adaptations, correlated with the highly specialised strücture of the adult. Many facts show that it is not worth while to attach much importance to so inconstant and variable a character as the arrangement of ciliated belts in pelagic larvæ. But if this point were of importance, their arrangement in Actinotrocha would not present any great difficulties in the way of regarding the creature as a true Gephyrean larva. If the circlet of swimming arms were reduced to a simple postoral belt and the præoral lobe reduced in size, the larva would agree fairly well with the larva of Phascolosoma or Boneilia. If, in support of this view, it is necessary to consider the longer cilia along the margin of the præoral lobe as representing a præoral belt comparable to that of the Echiurus larva, I see no valid objection to so considering them.

Accepting, then, the view that Phoronis is a true Gephyrean, we may note that among these animals two series of forms may be distinguished, which differ from each other in the course of the alimentary canal and the position of the anus. This division of the group is not necessarily a “natural” one; for our present purpose this point is quite immaterial. In one series, represented by such forms as Boneilia, Thalassema, Echiurus, the mouth and anus are at opposite extremities of the body, and the alimentary canal, aside from secondary flexures, pursues a straight course from one to the other. In the other series, including Phascolosoma, Sipunculus, Phoronis, and others, the anus is near the mouth on the apparently dorsal side of the body; and the alimentary canal is bent upon itself to form a long U-shaped loop, which is usually complicated by secondary flexures, as in the first series. The Actinotrochan larva of Phoronis, aside from its specially acquired swimming apparatus, corresponds pretty closely with such a form as Thalassema, representing the first series. And the larva may itself fairly be taken as a representative of this series. The presence of swimming arms is no obstacle to this view, for these are, clearly, provisions to increase the surface for the attachment of locomotor cilia, and can have no ancestral significance.¹

Through its metamorphosis the larva becomes an extreme representative of the second series, the anus undergoing, apparently, a transfer from one extremity of the body to a point very near the opposite extremity, beside the mouth, and the intestine acquiring a corresponding flexure.

From these and other more general considerations, it is evident that the displacement of the anus and corresponding flexure among the Gephyrea in general are derivative characters which, in all probability, were originally acquired to adapt the animals more perfectly to a tubicolous life. We have seen how this shifting of the anus is effected in the individual development or ontogeny of the animal; and it is plain that in considering how this mothod of development has been acquired, the first question to answer is as to how this shifting was effected in past time during the phylogeny, as the ancestors of the animal passed from a free-swimming, or at least wandering, mode of life to a strictly sedentary tubicolous one.

The answers to this question are possible. The first is that the anus gradually moved dorsalwards, and then forwards to its present position behind the mouth. The second, which is the view here maintained, is that the worm upon assuming the tubicolous mode of life developed a habit of bending the body into a U-shape, bringing the posterior part of the body alongside the anterior part in order to discharge the excreta at the mouth of the tube, or for some similar reason. External signs of this flexure becoming in time obliterated by coalescence of the two limbs of the U, the body once more assumed a straight linear form, but with the anus and mouth now near the same extremity.

Obviously, there are many difficulties in the way of the supposition that the anus gradually moved forwards along the dorsal side. This process seems impossible if we assume the worm to have meanwhile retained its tubicolous habit; for only a very great displacement could be of any advantage, and it is impossible to suppose that such a displacement could occur as a natural variation of structure. To assume an intermediate mode of life during which the creature should live, for instance, in mud or sand, would not obviate this difficulty, but would do away with the need for any displacement at all. The existence of forms like Phascolosoma, which live in sand or mud, and yet have a greatly displaced anus, does not meet the objection; for there is some reason to believe that such forms may be considered descendants of strictly tubicolous forms which for some reason—perhaps increase of size—have abandoned their former mode of life.

On the other hand, the flexure hypothesis has considerable evidence in its favour. Among-the tubicolous Anue-lides there are forms—e. g. Sabellaria—which habitually flex the body, as I suppose the ancestors of Phoronis to have done. Such a form is shown in fig. 20, which represents a large Sabellaria from the North Carolina coast. It is very noteworthy that the direction of the flexure is constant and toward the dorsal aspect of the body; so that if in time external signs of the flexure should disappear, the anus would have exactly the same position it occupies in Phoronis, and the intestine would have the same disposition. Admitting that such a flexure took place, it seems very probable, a priori, that the two parts of the body thus brought into proximity would tend in time to coalesce, and thus to destroy the appearance of flexure. In certain analogous cases such a flexure and fusion plainly seems to have occurred. A clear and convincing illustration is afforded by certain Holothurians; for here a record of the change has been preserved in the rows of ambulacral suckers. These retain their flexed course, and thus give us external evidences of the history of the animal, which are wanting in Phoronis. Such forms as Pentacta or Synapta are perfectly straight, exhibit a striking though not absolutely perfect radial symmetry, and the radii of the body are of equal length. In other forms, like Cucumaria, which, living in sand, habitually bend the body sharply in the middle to bring both extremities to the surface, the body has lost something of its radial symmetry. The side of the body towards which the flexure is made is perceptibly shorter than the other, and the body cannot be fully straightened. In other words, the flexure is partially obliterated by coalescence of the body walls, it has become organic. Here, again, the direction of the flexure is constant, being towards the biviurn. A further step is seen in forms like Psolus or Lophothuria, where the radial symmetry has become profoundly modified, and the mouth and cloaca are perhaps twice as far apart on the side of the trivium as on the opposite side. Whether the next stage, which would be in shape something like an Ascidian, exists among the Holothurians I do not know. But the extreme of the series is found in Rhopalodina, where the mouth and cloacal opening are in immediate proximity, and the body is considerably elongated in a direction transverse to the original long axis. That this structure was really brought about by the complete flexure of a primitively straight and radially symmetrical form is shown by the persistence of this flexure, almost unaltered in the ambulacral vessels, at first pointed out by Hermann Ludwig.

Another illustration is afforded by the Chætopod larva Mitraría. In this well-known form the digestive tube is completely doubled upon itself, so that the mouth and anus are in immediate proximity. We must believe that here, too, the entire body has undergone an actual or virtual-flexure corresponding to that of the intestine; for in a later stage a deep infolding of the body wall grows in between the mouth and anus, so that the previously concealed flexure becomes apparent. It may be added that the flexure subsequently straightens out and the worm assumes the ordinary form. This mode of development is the converse of what I take to have been the ancestral history of Phoronis.

These facts are not very full, yet they are enough to demonstrate the possibility of such a process of transformation as that which has been assumed to have taken place among the Gephyrea. The case would be stronger if there were in existence any forms intermediate between the two series of Gephyrean forms. But it must be admitted that no such forms are now known. In certain species, it is true, the mouth and anus are much more widely separated than in Phoronis. These forms show no external evidences of any flexure of the body; and if they were really intermediate forms their structure would furnish a strong argument against the flexure hypothesis. But it must be noted that in many of these forms the anterior or oral part of the body walls may be invaginated to form a sort of false oesophagus with the true mouth at its bottom. And it seems probable that the considerable interval between the mouth and anus exists simply in order to permit such invagination to take place without involving the latter opening. If this surmise be correct, the forms in question have really been derived from others which had the mouth and anus closely approximated, and therefore they are not intermediate forms at all, and present no difficulties in the way of the view which has been advanced.

Assuming, then, that the peculiar structure of Phoronis has resulted from the flexure of a primitively straight form, we may proceed to a consideration of the metamorphosis as viewed in this light. In the first place, what general causes have rendered this sudden and violent metamorphosis serviceable to the animal ? The answer lies in the circumstance that the animal is subjected, during its larval existence, to conditions of life utterly unlike those by which it is surrounded when adult. At first pelagic and actively free-swimming, it subsequently assumes a purely sedentary mode of life, inhabiting a fixed tube which it never leaves, and in which movement is limited to comparatively sluggish extensions and contractions of the body. In passing from one existence to the other the animal must undergo a complete revolution in its mode of life; as a matter of course, this profound change can be possible only if accompanied by a corresponding modification of structure. In fact, the larva and adult are extremely different in appearance and in structure. Each is very perfectly adapted to its own special set of conditions; and since the two sets of conditions are very unlike, the corresponding structural adaptations are also very unlike. Now the animal must somehow exchange the one set of characters for the other; and of course the most advantageous method of exchange will be preserved. If the larva were converted into the adult by a process of continuous growth, gradually losing its larval peculiarities while acquiring the adult feature, evidently an intermediate or transition period would result, during which the animal would be imperfectly adapted to either larval or adult life, and yet would require all its energies to keep up the structural changes going on. It would either be at a great disadvantage during this period or would have to acquire still another set of compensating adaptations answering to the requirements of the transition stage. Examples of such adaptations are common, e. g. among many insects where the changes undergone are so profound, apparently, as to render transition stages inevitable.

For these reasons, it seems manifest that it would be advantageous for the animal to pass rapidly and directly from the larval structure to the adult, thus escaping as far as possible the disadvantages entailed by a state of transition or the expenditure of energy demanded by the acquisition of secondary adaptations. The metamorphosis of Actino-trocha secures to it this advantage, and it seems clear that this is why the process of sudden transformation has been acquired.

Passing on now to consider how the process may have been acquired, the bearing of the speculations concerning the way in which the anus originally left its primitive terminal position becomes apparent. If my theory of this process is correct, it is evident that in the adult worm the dorsal region is nearly obliterated, being represented only by the short interval between the mouth and the anus; while the ventral region includes nearly the whole length of what is apparently the dorsal surface as well as the whole “ventral “surface. In the larva, however, the dorsal and ventral region are of nearly equal extent; so that in assuming the adult condition the ventral region must undergo extensive increase through some process of growth. From what has been said above, it is evident that advantage would be derived if this growth could take place in such a way as not to impair the adaptation of the larva to its conditions of life. A simple ventral outgrowth of the body wall, carrying with it a loop of the intestine, would destroy the balance of the larval body, render the præanal belt of cilia useless, and increase the size of the body, so that the swimming apparatus would be insufficient, and the pelagic life would have to be abandoned for a period of transition. On the other hand, if the ventral wall, as it grew, should become so folded on itself as to preserve the outlines of the body unaltered, an extensive growth would be possible, without the need for any transition period. Abundant room for such an infolding is afforded by the spacious perivisceral cavity of Actinotrocha, and the pouch may be regarded as having been derived in this way. Strictly parallel cases among other animals are not numerous. Perhaps an imperfect illustratration may be drawn from the foldings in the embryonic wings of insects which render them capable of being stowed away in a very small space in the pupa, and yet permit their rapid expansion at the time when the imago state is assumed.

A much more striking instance is afforded by the metamorphosis of certain Polyzoa. We owe to Barrois (see ‘Annales des Sciences Naturelles,’August, 1880) the very interesting observations that the so-called “internal sac,” which has been considered as the rudiment of some portion of the alimentary canal, becomes evaginated at the time of metamorphosis and then forms a large peduncle (plague quadrangulaire), by means of which the larva first attaches itself. The similarity of this process to the metamorphosis of Actinotrocha is obvious; and it seems equally clear that it has arisen for the same reason. The larval Polyzoon thus makes ready for the act of attachment without detriment to its own adaptation to free-swimming life.

The infolding in the larvæ of the ancestors of Phoronis must have been at first slight and more or less indefinite, becoming more extensive and definite as the dorsal region of the adult diminished in consequence of the gradual obliteration of the flexure. From such a primitive infolding the pouch of Actinotrocha could by natural selection be readily derived. The external opening would tend to become restricted for the exclusion of parasites or foreign bodies, and the gradual deepening of the infolding would at length reduce it to the form of a long pouch. The fibrous or muscular connection between the pouch and the walls of the alimentary canal are perhaps homologous with some of the.similar fibres connecting the stomach wall and body wall in such Gephyrea as Thalassema or Boneilia, which are in turn comparable to the septa of the Annelides.

A little consideration shows that the metamorphosis itself is in reality a sudden and extreme dorsal flexure of the body, which may be considered as the ontogenetic repetition of a habit of adult ancestral forms. It differs from the latter, however, in the immediate disappearance of external signs of the flexure, while in the phylogeny this disappearance probably took place very gradually. Fig. 13 shows the larval body bent at right angles towards the dorsal side.

A few further remarks may be added in regard to the systematic position of Phoronis. Its very striking resemblance to a simple hippocrepian Polyzoon is entirely secondary, and is a very curious illustration of the acquisition of almost exactly similar structures to meet similar conditions by organisms having no near genetic relation. As already stated, the Polyzoon-like character is a result of strictly tubicolous life; and the latter, again, may depend in part upon the absence of structures, like the complex setæ of tubicolous Annelides, adapted to effect the ready protrusion or withdrawal of the body. Schneider’s comparison of Actinotrocha to the Polyzoon larva Cyphonautes is purely superficial, and affords no proof whatever of relationship between the Polyzoa and Gephyrea. Further, his notion of the relation of Phoronis to its larva, which he compares to that existing between the polyzoon polypide and the cystid from which it develops, is manifestly based on a misunderstanding of the real nature of the metamorphosis, for the adult cannot be said, in any sense, to arise by a process of gemmation upon the larva.

The significance of the life-history of Phoronis becomes apparent when we pass to a consideration of some of the remarkable metamorphoses undergone by other animals. As already pointed out, these metamorphoses are in most cases of so complex a character that it is impossible to follow out in imagination their past history as circumstantially as we are able to follow the history of Phoronis. Nevertheless, we can trace the same principle in many of these cases, and in a few instances a somewhat similar process. For example, in the well-known and very remarkable case of Pilidium the animal is subjected, during its development, to two entirely different environments. During the earlier part of its life it is, like Actinotrocha, an active free-swimming animal. At a later period it leads an utterly different life, burrowing in mud or sand, living upon different food with new enemies, and subjected to many other new influences. Correlated with these great differences of environment we find so great a difference of structure between the larva and the adult that no one, without knowing the development, could suspect their identity. They are of wholly unlike shape, have acquired independent and dissimilar sensory and locomotor organs, protective characters, and possibly even distinct nervous systems. Notwithstanding these very great differences, the peculiar development of the Nemertine within the larval body obviates entirely the necessity for intermediate stages with their attendant disadvantages, and permits what may fairly be called an instantaneous leap from one condition of adaptation to another. As in the case of Actinotrocha, a complete preparation for the adult condition is gradually made, by the formation of a large part of the adult structure from portions of the larval body wall, which are infolded into the perivisceral cavity, and there go on developing without altering the external features of the larva. There are four such invaginations in Pilidium, and they undergo much more profound and extensive structural changes than does the single invagination of Actinotrocha. Yet it seems to me that they may have had a not very unlike origin. It is tolerably clear that the same general cause has determined their development, and I think the two processes of growth may be classed together.

We find something similar, again, among the Echinoderms, which are especially interesting as exhibiting a series of larval forms undergoing various degrees of metamorphosis. Here, too, in some cases, when the metamorphosis is very decided, the first rudiment of the adult arises from an infolding of the larval body wall, though more commonly no such invagination occurs. But in either case the adult develops within the body of the larva in such a way as to preserve almost unaltered those external features of the latter, by means of which it comes into direct relations with the surrounding medium. The tendency is towards the avoidance or abbreviation of transition stages by maintaining the larval adaptation unimpaired as long as possible. In this case transition stages are not entirely avoided, for it seems impossible to quite bridge over in this way the very great structural differences between the larva and the adult.

It is a significant fact that the development of the Holothurians is simpler and more direct than that of the Starfish, Sea-urchins, or Ophiurans. This seems to depend on the fact that the adults of the former group are soft-bodied, with flexible walls, and not very different in shape from the larvæ. Thus, a direct transformation of the larvæ into the adults is possible without the intervention of a very prolonged or distinct intermediate stage, while the rigid and regular coverings of the other groups involves a greater metamorphosis of the larva, which accordingly seems to require more gradual preparation. This can be made only during a period of transition or by means of some special mode of internal development. And the latter method, being more advantageous, has been acquired and preserved. To trace out exactly how this process has been acquired seems impracticable at present, owing to the want of sufficiently minute and extended knowledge of the exact conditions of the larval and adult life. But it seems quite possible that a complete explanation of these interesting phenomena will in time become possible on this principle of the abbreviation of transition stages.

The significance of insect metamorphoses has been so well elucidated, that I will add only a few words on this subject. In this group the structural differences between larva and adult are, in many cases, of such a nature that a transition stage cannot be avoided; and we find this stage provided, in many cases, with the most elaborate adaptive structures to compensate for the disadvantage thus necessitated. It is a very interesting fact, as Mr. Balfour well remarks, that the intermediate (pupa) stage as thus protected “has become secondarily adapted to play a part in the economy of the species quite different from that to which it owes its origin,” i. e. the protection of the creature during the inclement season of the year, as when the insect passes the winter in the pupa state.

Although a transition stage occurs, it is ordinarily assumed, so far as external features are concerned, by a sudden change and not by gradual modification of the larva; and the change from pupa to imago is equally abrupt. Sir John Lubbock’s explanation of the suddenness of these changes is that it results from the hardness of the external skin, which renders gradual modification impossible. This is clear enough in the change from pupa to imago, but it seems insufficient to explain the sudden change from the soft-skinned larva to the pupa. This is rather to be explained as a result of the advantage of maintaining complete adaptation to larval life up to as late a period as possible. It is very interesting to note that in some cases of decided metamorphosis the abruptness of change is facilitated by the development of portions of the adult organism from invaginations of the larval skin—the imaginal discs—so that an internal preparation is made by a process which has analogies with the development of Actinotrocha, Pilidium, and Echinoderms, and may have had a somewhat similar origin. The infoldings undergo so complex changes and become so highly specialised in the insects (as in Pilidium) that it is not easy from a consideration of their development in this group alone to understand how they at first arose. But the simplicity of the process in Actinotrocha renders it possible to suppose that the imaginal discs of insects may be the result of the gradual complication of simple infoldings of the body wall, first acquired, as in Actinotrocha, to preserve the larval external form.

The general conclusions to which a study of these phenomena of metamorphosis leads may be thus stated. Abrupt metamorphosis has resulted from the advantage derived from the abbreviation or avoidance of periods of imperfect adaptation. It is effected through acceleration of the development of certain portions of the larval organism with reference to a future adult state, while the remaining portions are specialised to meet the conditions of larval life. The organism thus becomes specialised simultaneously in two divergent directions, and in such a way that the two courses of development do not interfere with each other. The metamorphosis consists in a sudden assumption of functional activity by the adult set of structures and the simultaneous cessation or transformation of activity in the larval set. This may be effected either by rapidly absorbing or bodily casting off the larval structures or by a more or less complete transformation of them into adult structures; while a greater or less number of larval structures may persist nearly unaltered as the corresponding structures of the adult.

I gladly avail myself of this opportunity to make my acknowledgments to Dr. Brooks for his constant aid and counsel both to myself and to my fellow workers at the Zoological Laboratory.