Chapter XV: Final Remarks (5)

The evidence, then, of Ammocoetes is very conclusive. Originally a tube composed of a single layer of epithelial cells became expanded at the anterior end to form a bulb. On the outside of this tube or stalk the fibres of the optic nerve make their appearance, arising from the ganglion-cell layer of the retina, and, passing over the surface of the epithelial tube at the choroidal fissure, proceed to the brain by way of the optic chiasma. Owing to the large number of fibres, their crossing at the junction of the stalk with the bulb, and the narrowness at this neck, the obliteration of the lumen of the tube which takes place in the stalk is carried out to a still greater extent at this narrow part. The result of this is that all continuity of the cell-layers of the original tube of the optic stalk with those of both the inner and outer walls of the bulb is interrupted, and all that remains in this spot of the original continuous line of cells which connected the tube of the stalk with that of the bulb are possibly some of the groups of cells which are found scattered among the fibres of the optic nerve at their entrance into the retina. Such separation of the originally continuous elements of the epithelial wall of the optic stalk, which is apparent only at this neck of the nerve in Petromyzon, takes place {107}along the whole of the optic nerve in the higher vertebrates, so that no continuous axial core of cells exist, but only scattered supporting cells.

If further proof in support of this view be wanted, it is given by the evidence of physiology, which shows that the fibres of the optic nerve are not different from other nerve-fibres of the central nervous system, but that they degenerate when separated from their nerve-cell, and that the nerve-cell of which the optic nerve-fibre is a process is the large ganglion-cell of the ganglionic layer of the retina. The origin of the ganglionic layer of the retina cannot therefore be separated from that of the optic nerve-fibres. If the one is outside the epithelial tube, so is the other, and what holds true of the ganglionic layer must hold good of the rest of the retinal ganglion and, from all that has been said, of the retina itself. We therefore come to the conclusion that the evidence is distinctly in favour of the view, that the retina and optic nerve in the true sense are structures which originally were outside a non-nervous tube, but, just like the central nervous system as a whole, have amalgamated so closely with the elements of this tube as to utilize them for supporting structures. One part of this non-nervous tube, its dorsal wall, like the corresponding part of the brain-tube, still retains its original character, and by the deposition of pigment has been pressed into the service of the eye to form the pigmented epithelial layer.

We can, however, go further than this, for we know definitely in the case of the retina what the fate of the epithelial cells lining this tube has been. They have become the system of supporting structures known as Müllerian fibres.

The epithelial layer of the primary optic vesicle can be traced into direct continuity with the lining epithelium of the brain cavity, as a single layer of epithelial cells in the core of the optic nerve, forming the optic stalk, which, in consequence of close contact, becomes the well-known axial layer of supporting cells. This epithelial layer of the optic stalk then expands to form the optic bulb, the outer or dorsal wall of which still remains as a single layer of epithelium and becomes the layer of pigment epithelium. This layer of epithelium becomes doubled on itself by the approximation of the inner or ventral wall of the optic cup to the outer or dorsal wall in consequence of the presence of the lens, and still remaining a single layer, forms the _pars ciliaris retinæ_; then suddenly, at the _ora {108}serrata_, the single epithelial layer vanishes, and the layers of the retina take its place. It has long been known, however, that even throughout the retina this single epithelial layer still continues, being known as the fibres of Müller. This is how the fact is described in the last edition of Foster's "Text-book of Physiology," p. 1308--

"Stretching radially from the inner to the outer limiting membrane in all regions of the retina are certain peculiar-shaped bodies known as the radial fibres of Müller. Each fibre is the outcome of the changes undergone by what was at first a simple columnar epithelial cell. The changes are, in the main, that the columnar form is elongated into that of a more or less prismatic fibre, the edges of which become variously branched, and that while the nucleus is retained the cell substance becomes converted into neuro-keratin. And, indeed, at the _ora serrata_ the fibres of Müller may be seen suddenly to lose their peculiar features and to pass into the ordinary columnar cells which form the _pars ciliaris retinæ_."

_O.n._, axial core of cells in optic nerve; _p._, pigment epithelium; _p.c.r., pars ciliaris retinæ_; _m.f._, Müllerian fibres; _l._, lens.]

It is then absolutely clear that the essential parts of the eye may be considered as composed of two parts--

1. A tube or diverticulum from the tube of the central nervous system, composed throughout of a single layer of epithelium, which forms the supporting axial cells in the optic nerve, the pigment epithelium and the Müllerian fibres of the retina. Such a tube would be represented by the accompanying Fig. 44, and the left side of Fig. 41.

2. The retina proper with the retinal ganglion and the optic nerve-fibres as already described. In this part supporting elements are found, just as in any other compound retina, of the nature of neuroglia, which are independent of the Müllerian fibres.

{109}Of these two parts we have already seen that the second is to all intents and purposes a compound retina of a crustacean eye, and seeing that the single-layered epithelial tube is continuous with the single-layered epithelial tube of the central nervous system--_i.e._ with the cephalic part of the gut of the arthropod ancestor--it follows with certainty that the ancestor of the vertebrates must have possessed two anterior diverticula of the gut, with the wall of which, near the anterior extremity, the compound retina has amalgamated on either side, just as the infra-oesophageal ganglia have amalgamated with the ventral wall of the main gut-tube. In this way, and in this way alone, does the interpretation of the structure of the vertebrate lateral eye harmonize in the most perfect manner with the rest of the conclusions already arrived at.

The question therefore arises:--Have we any grounds for believing that the ancient forms of primitive crustaceans and primitive arachnids, which were so abundant in the time when the Cephalaspids appeared, possessed two anterior diverticula of the stomach, such as the consideration of the vertebrate eye strongly indicates must have been the case?

The beautiful pictures of Blanchard, and his description, show how, on the arachnid side, paired diverticula of the stomach are nearly universal in the group. Thus, although they are not present in the scorpions, still, in the Thelyphonidæ, Phrynidæ, Solpugidæ, Mygalidæ, the most marked characteristic of the stomach-region is the presence of four pairs of coecal diverticula, which spread laterally over the prosomatic region. In the spiders the number of such diverticula increases, and the whole prosomatic region becomes filled up with these tubes. Blanchard considers that they form nutrient tubes for the direct nutrition of the organs in the prosoma, especially the important brain-region of the central nervous system. He points out that these animals are blood-suckers, and that, therefore, their food is already in a suitable form for purposes of nutrition when it is taken in by them, so that, as it were, the anterior part of the gut is transformed into a series of vessels or diverticula conveying blood directly to the important organs in the prosoma, by means of which they obtain nourishment in addition to their own blood-supply.

The universality of such diverticula among the arachnids makes it highly probable that their progenitors did possess an alimentary canal with one or more pairs of anterior diverticula. In the {110}vertebrate, however, the paired diverticula are associated with a compound retina, a combination which does not occur among living arachnids; we must, therefore, examine the crustacean group for the desired combination, and naturally the most likely group to examine is the Phyllopoda, especially such primitive forms as Branchipus and Artemia, for it is universally acknowledged that these forms are the nearest living representatives of the trilobites. If, therefore, it be found that the retina and optic nerve in Artemia is in specially close connection with an anterior diverticulum of the gut on each side, then it is almost certain that such a combination existed also in the trilobites.

The section is through the extreme anterior end of the diverticulum, thus cutting through many of the columnar cells at right angles to their axis. _Al._, gut diverticulum; _rt. gl._, retinal ganglion.]

{111}

_Br._, brain; _l.e._, lateral eyes; _c.e._, median eyes; _Al._, alimentary canal.]

_R._, retina; _l._, lens; _O.n._, optic nerve fibres; _Al._, cephalic end of invertebrate alimentary canal; _V._, cavity of ventricles of brain; _Al.d._, anterior diverticulum of alimentary canal; _op.d._, optic diverticulum.]

My friend Mr. W. B. Hardy has especially investigated the nervous system of Artemia. In the course of his work he cut serial sections through the whole animal, and, as mentioned in my paper in the _Journal of Anatomy and Physiology_, he discovered that the retinal ganglion of each lateral eye is so closely attached to the end of the corresponding diverticulum of the gut that the lining cells of the ventral part of the diverticulum form a lining to the retinal ganglion (Fig. 45). In this animal there are only two gut-diverticula, which are situated most anteriorly. I have plotted out this series of sections by means of a camera lucida, with the result that the retina appears as a bulging attached ventro-laterally to the extremity of each gut-diverticulum, as is shown in Fig. 46. It is instructive to compare with this figure Scott's picture of the developing eye in Ammocoetes, where he figures the retina as {112}a bulging attached ventrally to the extremity of the narrow tube of the optic diverticulum. In Fig. 47, A, I reproduce this figure of Scott, and by the side of it, Fig. 47, B, I have represented the origin of the vertebrate eye as I believe it to have occurred.

We see, then, this very striking fact, that in the most primitive of the Crustacea, not only are there two anterior diverticula of the gut, but also the retinal ganglion of the lateral eye is in specially close connection with the end of the diverticulum on each side. In fact, we find in the nearest living representative of the trilobites a retina and retinal ganglion and optic nerve, closely resembling that of the vertebrate, in close connection with an epithelial tube which has nothing to do with the organ of sight, but is one of a pair of anterior gut-diverticula. It is impossible to obtain more decisive evidence that the trilobites possessed a pair of gut-diverticula surrounded to a greater or less extent by the retina and optic nerve of each lateral eye.

Such anterior diverticula are commonly found in the lower Crustacea; they are usually known by the name of liver-diverticula, but as they take no part in digestion, and, on the contrary, represent that part of the gut which is most active in absorption, the term liver is not appropriate, and it is therefore better to call them simply the pair of anterior diverticula. Our knowledge of their function in Daphnia is given in a paper by Hardy and M^cDougall, which does not appear to be widely known. Hardy succeeded in feeding Daphnia with yolk of egg in which carmine grains were mixed, and was able in the living animal to watch the whole process of deglutition, digestion, and absorption. The food, which is made into a bolus, is moved down to the middle region of the gut, and there digestion takes place. Then by an antiperistaltic movement the more fluid products of the digestion-process are sent right forward into the two anterior diverticula, where the single layer of columnar cells lining these diverticula absorbs these products, the cells becoming thickly studded with fat-drops after a feed of yolk of egg. The carmine particles, which were driven forward with the proteid- and fat-particles, are not absorbed, but are at intervals driven back by contractions of the anterior diverticula to the middle region of the gut.

These observations prove most clearly that the anterior diverticula have a special nutrient function, being the main channels by which new nutrient material is brought into the body, and, as {113}pointed out by the authors, it is a remarkable exception in the animal kingdom that absorption should occur in that portion of the gut which is anterior to the part in which digestion occurs. In all these animals the two anterior diverticula extend forwards over the brain, and, as we have seen in Artemia, the anterior extremity of each one is so intimately related to a part of the brain--viz. the retinal ganglion--as to form a lining membrane to that mass of nerve-cells. It follows, therefore, that the nutrient fluid absorbed by the cells of this part of the gut-diverticulum must be primarily for the service of the retinal ganglion. In fact, the relations of this anterior portion of the gut to the brain as a whole suggest strongly that the marked absorptive function of this anterior portion of the gut exists in order to supply nutrient material in the first place to the most vital, most important organ in the animal--the brain and its sense-organs. This conclusion is borne out by the fact that in these lower crustaceans the circulation of blood is of a very inefficient character, so that the tissues are mainly dependent for their nutrition on the fluid immediately surrounding them. It stands to reason that the establishment of the anterior portion of the gut as a nutrient tube to the brain would necessitate a closer and closer application of the brain to that tube, so that the process of amalgamation of the brain with the single layer of columnar epithelial cells which constitutes the wall of the gut (which we see in its initial stage in the retinal ganglion of Artemia), would tend rapidly to increase as more and more demands were made upon the brain, until at last both the supra- and infra-oesophageal ganglia, as well as the retinal ganglia and optic nerves, were in such close intimate connection with the ventral wall of the anterior portion of the gut and its diverticula as to form a brain and retina closely resembling that of Ammocoetes.

Such an origin for the lateral eyes of the vertebrate explains in a simple and satisfactory manner why the vertebrate retina is a compound retina, and why both retina and optic nerve have an apparent tubular development.

At the same time one discrepancy still exists which requires consideration--viz. in no arthropod eye possessing a compound retina is the retina inverted. All the known cases of inversion among arthropods occur in eyes, the retina of which is simple, and are all natural consequences of the process of invagination by which {114}the retina is formed. On the other hand, eyes with an inverted compound retina are not entirely unknown among invertebrates, for the eyes of Pecten and of Spondylus possess a retina which is inverted after the vertebrate fashion and still may be spoken of as compound rather than simple. It is clear that an invagination, the effect of which is an inversion of the retinal layer, would lead to the same result, whether the retinal optic nerves were short or long, whether, in fact, a retinal ganglion existed or not. Undoubtedly the presence of the retinal ganglion tends greatly to obscure any process of invagination, so that, as already mentioned, many observers, with Parker, consider the retina of the crustacean lateral eye to be formed by a thickening only, without any invagination, while Reichenbach says an obscure invagination does take place at a very early stage. So in the vertebrate eye most observers speak only of a thickening to form the retina, but Götte's observation points to an invagination of the optic plate at an early stage. So also in the eye of Pecten, Korschelt and Heider consider that the thickening, by which the retina is formed according to Patten, in reality hides an invagination process by means of which, as Bütschli suggests, an optic vesicle is formed in the usual manner. The retina is formed from the anterior wall of this vesicle, and is therefore inverted.

The origin of the inverted retina of the vertebrate eye does not seem to me to present any great difficulty, especially when one takes into consideration the fact that the retina is inverted in the arachnid group, only in the lateral eyes. The inversion is usually regarded as associated with the tubular formation of the vertebrate retina, and it is possible to suppose that the retina became inverted in consequence of the involvement of the eye with the gut-diverticulum. I do not myself think any such explanation is at all probable, because I cannot conceive such a process taking place without a temporary derangement--to say the least of it--of the power of vision, and as I do not believe that evolution was brought about by sudden, startling changes, but by gradual, orderly adaptations, and as I also believe in the paramount importance of the organs of vision for the evolution of all the higher types of the animal kingdom, I must believe that in the evolution from the Arthropod to the Cephalaspid, the lateral eyes remained throughout functional. I therefore, for my own part, would say that the inversion of the {115}retina took place before the complete amalgamation with the gut-diverticulum, that, in fact, among the proto-crustacean, proto-arachnid forms there were some sufficiently arachnid to have an inverted retina, and at the same time sufficiently crustacean to possess a compound retina, and therefore a compound inverted retina after the vertebrate fashion existed in combination with the anterior gut-diverticula. Thus, when the eye and optic nerve sank into and amalgamated with the gut-diverticulum, neither the dioptric apparatus nor the nervous arrangements would suffer any alteration, and the animal throughout the whole process would possess organs of vision as good as before or after the period of transition.

Further, not only the retina but also the dioptric apparatus of the vertebrate eye point to its origin from a type that combined the peculiarities of the arachnids and the crustaceans. In the former it is difficult to speak of a true lens, the function of a lens being undertaken by the cuticular surface of the cells of the corneagen (Mark's 'lentigen'), while in the latter, in addition to the corneal covering, a true lens exists in the shape of the crystalline cones. Further, these crustacean lenses are true lenses in the vertebrate sense, in that they are formed by modified hypodermal cells, and not bulgings of the cuticle, as in the arachnid. We see, in fact, that in the compound crustacean eye an extra layer of hypodermal cells has become inserted between the cornea and the retina to form a lens. So also in the vertebrate eye the lens is formed by an extra layer of the epidermal cells between the cornea and the retina. The fact that the vertebrate eye possesses a single lens, though its retina is composed of a number of ommatidia, while the crustacean eye possesses a lens to each ommatidium, may well be a consequence of the inversion of the vertebrate retina. It is most probable, as Korschelt and Heider have pointed out, that the retina of the arachnid eyes is composed of a number of ommatidia, just as in the crustacean eyes and in the inverted eyes it is probable that the image is focussed on to the pigmented tapetal layer, and thence reflected on to the percipient visual rods. In such a method of vision a single lens is a necessity, and so it must also be if, as I suppose, eyes existed with an inverted compound retina. Owing to the crustacean affinities of such eyes, a lens would be formed and the retina would be compound: owing to the arachnid affinities, the retina would be inverted and the hypodermal cells which formed the lens would be massed {116}together to form a single lens, instead of being collected in groups of four to form a series of crystalline cones.

To sum up: The study of the vertebrate eyes, both median and lateral, leads to most important conclusions as to the origin of the vertebrates, for it shows clearly that whereas, as pointed out in this and subsequent chapters, their ancestors possessed distinct arachnid characteristics, yet that they cannot have been specialized arachnids, such as our present-day forms, but rather they were of a primitive arachnid type, with distinct crustacean characteristics: animals that were both crustacean and arachnid, but not yet specialized in either direction: animals, in fact, of precisely the kind which swarmed in the seas at the time when the vertebrates first made their appearance. In the opinion of the present day, the ancestral forms of the Crustacea, which were directly derived from the Annelida, may be classed as an hypothetical group the Protostraca, the nearest approach to which is a primitive Phyllopod.

"Starting from the Protostraca," say Korschelt and Heider, "according to the present condition of our knowledge, we may, as has been already remarked, assume three great series of development of the Arthropodan stock, by the side of which a number of smaller independent branches have been retained. One of these series leads through the hypothetical primitive Phyllopod to the Crustacea; the second through the Palæostraca (Trilobita, Gigantostraca, Xiphosura) to the Arachnida; the third through forms resembling Peripatus to the Myriapoda and the Insecta. The Pantapoda and the Tardigrada must probably be regarded as smaller independent branches of the Arthropodan stock."

To these "three great series of development of the Arthropodan stock" the evidence of Ammocoetes shows that a fourth must be added, which, starting also from the Protostraca, and closely connected with the second, palæostracan branch, leads through the Cephalaspidæ to the great kingdom of the Vertebrata. Such a direct linking of the earliest vertebrates with the Annelida through the Protostraca is of the utmost importance, as will be shown later in the explanation of the origin of the vertebrate coelom and urinary apparatus.

{117}SUMMARY.

The most important discovery of recent years which gives a direct clue to
the ancestry of the vertebrates is undoubtedly the discovery that the
pineal gland is all that remains of a pair of median eyes which must have
been functional in the immediate ancestor of the vertebrate, seeing how
perfect one of them still is in Ammocoetes. The vertebrate ancestor,
then, possessed two pairs of eyes, one pair situated laterally, the other
median. In striking confirmation of the origin of the vertebrate from
Palæostracans it is universally admitted that all the Eurypterids and
such-like forms resembled Limulus in the possession of a pair of median
eyes, as well as of a pair of lateral eyes. Moreover, the ancient mailed
fishes the Ostracodermata, which are the earliest fishes known, are all
said to show the presence of a pair of median eyes as well as of a pair
of lateral eyes. This evidence directly suggests that the structure of
both the median and lateral vertebrate eyes ought to be very similar to
that of the median and lateral arthropod eyes. Such is, indeed, found to
be the case.

The retina of the simplest form of eye is formed from a group of the
superficial epidermal cells, and the rods or rhabdites are formed from
the cuticular covering of these cells; the optic nerve passes from these
cells to the deeper-lying brain. This kind of retina may be called a
simple retina, and characterizes the eyes, both median and lateral, of
the scorpion group.

In other cases a portion of the optic ganglion remains at the surface,
when the brain sinks inwards, in close contiguity to the epidermal
sense-cells which form the retina; a tract of fibres connects this optic
ganglion with the underlying brain, and is known as the optic nerve. Such
a retina may be called a compound retina and characterizes the lateral
eyes of both crustaceans and vertebrates. Also, owing to the method of
formation of the retina by invagination, the cuticular surface of the
retinal sense-cells, from which the rods are formed, may be directed
towards the source of light or away from it. In the first case the retina
may be called upright, in the second inverted.

Such inverted retinas are found in the vertebrate lateral eyes and in the
lateral eyes of the arachnids, but not of the crustaceans.

The evidence shows that all the invertebrate median eyes possess a simple
upright retina, and in structure are remarkably like the right median or
pineal eye of Ammocoetes; while the lateral eyes possess, as in the
crustaceans, an upright compound retina, or, as in many of the arachnids,
a simple inverted retina. The lateral eyes of the vertebrates alone
possess a compound inverted retina.

This retina, however, is extraordinarily similar in its structure to the
compound crustacean retina, and these similarities are more accentuated
in the retina of the lateral eye of Petromyzon than that of the higher
vertebrates.

The evidence afforded by the lateral eye of the vertebrate points
unmistakably to the conclusion that the ancestor of the vertebrate
possessed both crustacean and arachnid characters--belonged, therefore,
to a group of animals which gave rise to both the crustacean and arachnid
groups. This is precisely the position of the Palæostracan group, which
is regarded as the ancestor of both the crustaceans and arachnids.
{118}In two respects the retina of the lateral eyes of vertebrates
differs from that of all arthropods, for it possesses a special
supporting structure, the Müllerian fibres, which do not exist in the
latter, and it is developed in connection with a tube, the optic
diverticulum, which is connected on each side with the main tube of the
central nervous system. These two differences are in reality one and the
same, for the Müllerian fibres are the altered lining cells of the optic
diverticulum, and this tube has the same significance as the rest of the
tube of the nervous system; it is something which has nothing to do with
the nervous portion of the retina but has become closely amalgamated with
it. The explanation is, word for word, the same as for the tubular
nervous system, and shows that the ancestor of the vertebrate possessed
two anterior diverticula of its alimentary canal which were in close
relationship to the optic ganglion and nerve of the lateral eye on each
side. It is again a striking coincidence to find that Artemia, which with
Branchipus represents a group of living crustaceans most nearly allied to
the trilobites, does possess two anterior diverticula of the gut which
are in extraordinarily close relationship with the optic ganglia of the
retina of the lateral eyes on each side.

The evidence of the optic apparatus of the vertebrate points most
remarkably to the derivation of the Vertebrata from the Palæostraca.

{119}CHAPTER III

_THE EVIDENCE OF THE SKELETON_

The bony and cartilaginous skeleton considered, not the
notochord.--Nature of the earliest cartilaginous skeleton.--The
mesosomatic skeleton of Ammocoetes; its topographical arrangement, its
structure, its origin in muco-cartilage.--The prosomatic skeleton of
Ammocoetes; the trabeculæ and parachordals, their structure, their origin
in white fibrous tissue.--The mesosomatic skeleton of Limulus compared
with that of Ammocoetes; similarity of position, of structure, of origin
in muco-cartilage.--The prosomatic skeleton of Limulus; the entosternite
or plastron compared with the trabeculæ of Ammocoetes; similarity of
position, of structure, of origin in fibrous tissue.--Summary.

The explanation of the two optic diverticula given in the last chapter accounts in the same harmonious manner for every other part of the tube around which the central nervous system of the vertebrate has been grouped. The tube conforms in all respects to the simple epithelial tube which formed the alimentary canal of the ancient type of marine arthropods such as were dominant in the seas when the vertebrates first appeared. The whole evidence so far is so uniform and points so strongly in the direction of the origin of vertebrates from these ancient arthropods, as to make it an imperative duty to proceed further and to compare one by one the other parts of the central nervous system, together with their outgoing nerves in the two groups of animals.

Before proceeding to do this, it is advisable first to consider the question of the origin of the vertebrate skeletal tissues, for this is the second of the great difficulties in the way of deriving vertebrates from arthropods, the one skeleton being an endo-skeleton composed of cartilage and bone, and the other an exo-skeleton composed of chitin. Here is a problem of a totally different kind to that we have just been considering, but of so fundamental a character that it must, if possible, be solved before passing on to the consideration of the cranial nerves and the organs they supply.

{120}Is there any evidence which makes it possible to conceive the method by which the vertebrate skeleton may have arisen from the skeletal tissues of an arthropod? By the vertebrate skeleton I mean the bony and cartilaginous structures which form the backbone, the cranio-facial skeleton, the pectoral and pelvic girdles, and the bones of the limbs. I do not include the notochord in these skeletal tissues, because there is not the slightest evidence that the notochord played any part in the formation of these structures; the notochordal tissue is something _sui generis_, and never gives rise to cartilage or bone. The notochord happens to lie in the middle line of the body and is very conspicuous in the lowest vertebrate; with the development of the backbone the notochord becomes obliterated more and more, until at last it is visible in the higher vertebrates only in the embryo; but that obliteration is the result of the encroachment of the growing bone-masses, not the cause of their growth. Although, then, the notochord may in a sense be spoken of as the original supporting axial rod of the vertebrate, it is so different to the rest of the endo-skeleton, has so little to do with it, that the consideration of its origin is a thing apart, and must be treated by itself without reference to the origin of the cartilaginous and bony skeleton.

THE COMMENCEMENT OF THE BONY SKELETON IN THE VERTEBRATE.

What is the teaching of the vertebrate? What evidence is there as to the origin of the bony skeleton in the vertebrate phylum itself?

The axial bony skeleton of the higher Mammalia consists of two parts, (1) the vertebral column with its attached bony parts, and (2) the cranio-facial skeleton. Of these two parts, the bony tissue of the first arises in the embryo from cartilage, of the second partly from cartilage, partly from membrane.

In strict accordance with their embryonic origin is their phylogenetic origin: as we pass from the higher vertebrates to the lower these structures can be traced back to a cartilaginous and membranous condition, so that, as Parker has shown, the cranio-facial bony skeleton of the higher vertebrates can be derived directly from a non-bony cartilaginous skeleton, such as is seen in Petromyzon and the cartilaginous fishes.

Balfour, in his "Comparative Embryology," states that the {121}primitive cartilaginous cranium is always composed of the following parts:--

1. A pair of cartilaginous plates on each side of the cephalic section of the notochord known as the parachordals (_pa.ch._, Fig. 49; _iv._, Fig. 48). These plates, together with the notochord (_ch._) enclosed between them, form a floor for the hind and mid-brain.

_ch._, notochord; _iv._, parachordals; _au._, auditory capsule; _py._, pituitary body; _tr._, trabecula; _ctr._, trabecular cornu; _pn._, pre-nasal cartilage; _ppg._, palato-pterygoid tract; _mn._, mandibular arch; _th.h._, first branchial arch; _VII.-XII._, cranial nerves.]

_ol._, olfactory sacs; _au._, auditory capsule; _py._, pituitary body; _pa.ch._, parachordal cartilage; _tr._, trabecula; _inf._, infundibulum; _pt.s._, pituitary space; _e._, eye.]

2. A pair of bars forming the floor for the fore-brain, known as the trabeculæ (_tr_). These bars are continued forward from the parachordals. They meet posteriorly and embrace the front end of the notochord, and after separating for some distance bend in again in such a way as to enclose a space--the pituitary space (_pt.s._). In {122}front of this space they remain in contact, and generally unite. They extend forward into the nasal region (_pn._).

3. The cartilaginous capsules of the sense organs. Of these the auditory (_au._) and the olfactory capsules (_ol._) unite more or less intimately with the cranial walls; while the optic capsules, forming the usually cartilaginous sclerotics, remain distinct.

The parachordals and notochord form together the basilar plate, which forms the floor for that section of the brain belonging to the primitive postoral part of the head, and its extent corresponds roughly to that of the basioccipital of the adult skull.

The trabeculæ, so far as their mere anatomical relations are concerned, play the same part in forming the floor for the front cerebral vesicle as do the parachordals for the mid- and hind-brain. They differ, however, from the parachordals in one important feature, viz. that except at their hinder end they do not embrace the notochord. The notochord always terminates at the infundibulum, and the trabeculæ always enclose a pituitary space, in which lies the infundibulum (_inf._) and the pituitary body (_py._).

In the majority of the lower forms the trabeculæ arise quite independently of the parachordals, though the two sets of elements soon unite.

The trabeculæ are usually somewhat lyre-shaped, meeting in front and behind, and leaving a large pituitary space between their middle parts. Into this space the whole base of the fore-brain primitively projects, but the space itself gradually becomes narrowed until it usually contains only the pituitary body.

The trabecular floor of the brain does not long remain simple. Its sides grow vertically upwards, forming a lateral wall for the brain, in which in the higher types, two regions may be distinguished, viz. an alisphenoidal region behind, growing out from what is known as the basisphenoidal region of the primitive trabeculæ, and an orbito-sphenoidal region in front, growing out from the presphenoidal region of the trabeculæ. These plates form at first a continuous lateral wall of the cranium. The cartilaginous walls which grow up from the trabecular floor of the cranium generally extend upwards so as to form a roof, though almost always an imperfect roof, for the cranial cavity.

The basi-cranial cartilaginous skeleton reduces itself always into trabeculæ and parachordals with olfactory and auditory cartilaginous capsules.

{123}In addition, a branchial skeleton exists, which consists of a series of bars known as the branchial bars, so situated as to afford support to the successive branchial pouches. An anterior arch known as the mandibular arch (Fig. 50, _Mn._), placed in front of the hyo-mandibular cleft, and a second arch, known as the hyoid arch (_Hy._), placed in front of the hyo-branchial cleft, are developed in all types; the succeeding arches are known as the true branchial arches (_Br._), and are only fully developed in the Ichthyopsida. In all cases of jaw-bearing (gnathostomatous) vertebrates the first arch has become a supporting skeleton for the mouth (Fig. 51), and in the higher vertebrates in combination with the second or hyoid arch takes part in the formation of the ear-bones.

_Tr._, trabecula; _Mn._, mandibular cartilage; _Hy._, hyoid arch; _Br_1._, first branchial arch; _Na._, olfactory sac; _E._, eye; _Au._, auditory capsule; _Hm._, hemisphere; _C_1_, _C_2_, _C_3_, cerebral vesicles.]

_cr._, cranium; _Br._, branchial arches; _Mn._ + _Hy._, mandibular and hyoid arches.]

The true branchial arches persist, to a certain extent, in the Amphibia, and become still more degenerated in the Amniota (reptiles, birds, and mammals) in correlation with the total disappearance of a branchial respiration at all periods of their life. {124}Their remnants become more or less important parts of the hyoid bone, and are employed solely in support of the tongue.

In no single animal is there any evidence that the foremost arch, the mandibular, is a true branchial arch. As low down as the Elasmobranchs it becomes divided into two elements which form respectively the upper and lower jaws; the hyoid arch, on the other hand, although it has altered its form and acquired the secondary function of supporting the mandibular arch, still retains its respiratory function.

The evidence afforded by the mode of formation of the skeletal tissues of vertebrates down to the Elasmobranchs indicates that the primitive cranial skeleton arose from two paired basal cartilages, the parachordals and trabeculæ, to which were attached respectively cartilaginous cases enclosing the organs of hearing and smell. In addition, the branchial portion of the cranial region was provided with cartilaginous bars arranged serially for the support of the branchiæ, with the exception of the foremost, the mandibular bar, which formed supporting tissues for the mouth--the upper and lower jaws.

Just as in past times the spinal nerves and the segments they supplied were supposed to represent the type on which the original vertebrate was built, so also the spinal vertebræ afforded the type of the segmented skeleton, and the anatomists of those days strove hard to resolve the cranio-facial skeleton into a series of modified vertebræ. Owing especially to the labours of Huxley, who showed that the segmentation in the head-region was essentially a segmentation due to the presence of branchial bars, this conception was finally laid to rest and nowadays it is admitted to be hopeless to resolve the cranium into vertebral segments. Still, however, the vertebrate is a segmented animal and its segmented nature is visible in the cranial region, so far as the skeletal tissues are concerned, in the shape of the series of branchial and visceral bars.

To this segmentation the name of 'branchiomeric' has been given, while that due to the presence of vertebræ is called 'mesomeric.'

As we have seen, the internal bony skeleton of the vertebrate commences as a cartilaginous and membranous skeleton. For this reason the preservation of such skeletons is impossible in the fossil form, unless the cartilage has become impregnated with lime salts, so that there is but little hope of ever obtaining traces of such {125}structures in the fossils of the Silurian age either among the vertebrate or invertebrate remains. Fortunately for this investigation there are still living on the earth two representatives of that age; on the invertebrate side Limulus, and on the vertebrate side Ammocoetes.

The Elasmobranchs represent the most primitive of the gnathostomatous vertebrates. Below them come the Agnatha, known as the cyclostomatous fishes or Marsipobranchii, the lampreys (Petromyzon) and the hag-fishes (Myxine).

The skeleton of Petromyzon (Fig. 52) consists of a cranio-facial skeleton composed of a cartilaginous unsegmented cranium, with the basal trabeculæ and parachordals and a series of branchial and visceral cartilaginous bars forming the so-called branchial basket-work; to these must be added auditory and nasal capsules. In contradistinction to this elaborate cranio-facial skeleton, the spinal vertebral skeleton is represented only by segmentally arranged small pieces of cartilage formed in the connective tissue dissepiments between segmented sheets of body-muscles (myotomes).

_na._, nasal capsule; _au._, auditory capsule; _nc._, notochord.]

But Petromyzon is derived from Ammocoetes by a remarkable process of transformation, and a most important part of that transformation is the formation of new cartilaginous structures. Thus we see that in Ammocoetes there is no sign of a cartilaginous vertebral column; at transformation the rudimentary vertebræ of Petromyzon are formed. In Ammocoetes the brain-case is a simple fibrous membranous covering; at transformation this becomes cartilaginous. In Ammocoetes there are no cartilaginous structures corresponding to the sub-ocular arches; these are all formed at transformation. It follows, that we can trace back the bony skeleton of the vertebrate head to the skeleton of Ammocoetes, and we may therefore conclude {126}that the primitive cartilaginous skeleton of the vertebrate consisted of the following structures (Fig. 53, B), viz. the branchial bars forming a basket-work, the trabeculæ and parachordals, the auditory and nasal capsules--a clear proof that the cranial skeleton is older than the spinal. Of these structures the branchial bars are the only evidently segmented parts.

A, Diagram of cartilaginous skeleton of Limulus. _Soft cartilage_, entapophysial ligaments, deep black; branchial bars simply hatched; _hard cartilage_, lateral trabeculæ of entosternite, netted; _Ph._, position of pharynx.

B, Diagram of cartilaginous skeleton of Ammocoetes. _Soft cartilage_, sub-chordal cartilaginous bands, deep black; branchial basket-work (first formed part), simply hatched; _hard cartilage_, cranio-facial skeleton, trabeculæ, parachordals and auditory capsules, netted; _Inf._, position of tube of infundibulum (old oesophagus).]

THE SOFT CARTILAGE OF THE BRANCHIAL SKELETON OF AMMOCOETES.

The study of Ammocoetes gives yet another clue to the nature of the earliest skeleton, for these two marked groups of cartilage--the branchial and basi-cranial--are characterized by a difference in structure as well as a difference in topographical position. J. Müller was the first to point out that these two sets of cartilages differ in appearance and constitution, and he gave to them the name of yellow and grey cartilage. Parker has described them fully under the terms soft and hard cartilage, terms which Schaffer has also used, and I shall also make use of them here. The whole of the branchial cartilaginous skeleton is composed of soft cartilage, while the basi-cranial skeleton, consisting of trabeculæ, parachordals, and auditory capsule, is composed {127}of hard cartilage, the only soft cartilage in this region being that which forms the nasal capsule, not represented in Fig. 53, B.

These two groups of cartilage arise independently, so that at first the basi-cranial system is quite separate from the branchial, and only late in the history of the animal is a junction effected between the branchial system and the trabeculæ and parachordals, an initial separation which is especially striking when we consider that in this animal all the cartilaginous structures of any one system are continuous: there is no sign of anything in the nature of joints.

Of these two main groups, the branchial cartilages are formed first in the embryo, a fact which suggests that they are the most primitive of the vertebrate cartilages, and that, therefore, the first true formation of cartilage in the invertebrate ancestor may be looked for in the shape of bars supporting the branchial mechanism. The evidence of the origin of the cartilaginous structures in Ammocoetes is given by Shipley in the following words:--

"The branchial bases are the first part of the skeleton to appear. They arise about the 24th day as straight bars of cartilage, lying external and slightly posterior to the branchial vessel.

"The first traces of the basi-cranial skeleton appear on the 30th day as two rods of cartilage--the trabeculæ."

Our attention must, in the first place, be directed to this branchial basket-work of Ammocoetes.

Underlying the skin of Ammocoetes in the branchial region is situated the sheet of longitudinal body-muscles, divided into a series of segments or myotomes, which forms the somatic muscles so characteristic of all fishes. This muscular sheet is depicted on the left-hand side of Fig. 54. It does not extend over the lower lip or over that part in the middle line where the thyroid gland is situated. In these parts a sheet of peculiar tissue known by the name of muco-cartilage lies immediately under the skin, covering over the thyroid gland and lower lip. The somatic muscular sheet with the superjacent skin can be stripped off very easily owing to the vascularity and looseness of the tissue immediately underlying it. When this is done the branchial basket-work comes beautifully into view as is seen on the right-hand side of Fig. 54. It forms a cage within which the branchiæ and their muscles lie entirely concealed.

This is the great characteristic of this most primitive form of the branchial cartilaginous bars and distinguishes it from the branchial {128}bars of other higher fishes, in that it forms a system of cartilages which lie external to the branchiæ--an extra-branchial system.

This branchial basket-work is simpler in Ammocoetes than in Petromyzon, and its actual starting-point consists of a main transverse bar corresponding to each branchial segment; from this transverse bar the system of longitudinal bars by which the basket-work is formed has sprung. These transverse bars arise from a cartilaginous longitudinal rod, situated close against the notochord on each side. These rods may be called the subchordal cartilaginous bands (Fig. 53), and, according to the observations of Schneider and others, each subchordal band does not form at first a continuous cartilaginous rod, but the cartilage is conspicuous only at the places where the transverse bars arise. In the youngest Ammocoetes examined by Schaffer, he could find no absolute discontinuity of the cartilage except between the first two transverse bars, but he says that the thinning between the transverse bars was so marked as to make it highly probable that at an earlier stage there was discontinuity. The whole system of branchial bars and subchordal rods is at first absolutely disconnected from the cranial system of trabeculæ and parachordals, and only later do the two systems join.

_Th._, thyroid gland; _M._, lower lip, with its muscles.]

These observations on Ammocoetes lead most definitely to the conclusion that the starting-point of the whole cartilaginous skeleton of the vertebrate consisted of a series of transverse cartilaginous bars, for the purpose of supporting branchial segments; these were connected with two axial longitudinal cartilaginous rods, which at first contained cartilage only near the places of junction of the branchial {129}bars. This system may be called the mesosomatic skeleton, as it is entirely confined to the branchial or mesosomatic region.

In addition to this primitive cartilaginous framework, which was formed for the support of the mesosomatic or respiratory segments, but at a slightly later period in the phylogenetic history, a separate cartilaginous system was formed for the support of the prosomatic segments, viz. the trabeculæ and parachordals with the auditory capsules: a system which was at first entirely separated from the mesosomatic, and, as we shall see, is more advanced in structure than the branchial system. Later still, the story is completed at the time of transformation to Petromyzon by the formation of the simple cartilaginous skull and the rudimentary vertebræ, the structure of which is also of a more advanced type.

THE STRUCTURE OF THE SOFT BRANCHIAL CARTILAGE.

Having considered the topographical position of the primitive branchial cartilaginous skeleton, we may now inquire, What was its structure and how was it formed?

In the higher vertebrates various forms of cartilage are described, viz. hyaline, fibro-cartilage, elastic cartilage, and parenchymatous cartilage. Of these, the parenchymatous cartilage is looked upon as the most primitive form, because it preserves without modification the characters of embryonic cartilage.

Embryology, then, would lead to the belief that the earliest form of cartilage in the vertebrate kingdom ought to be of this type, viz. large cells, each of which is enclosed in a simple capsule, so that the capsules of the cells form the whole of the matrix, and thus form a simple homogeneous honeycomb-structure, in the alveoli of which the cartilage-cells lie singly. If, then, the branchial cartilages of Ammocoetes are, as has just been argued, the representatives of the cartilaginous skeleton of the primitive vertebrate, it is reasonable to suppose that they should resemble in structure this embryonic cartilage. Such is undoubtedly the case: all observers who have described the branchial basket-work of Ammocoetes or Petromyzon have been struck with the extremely primitive character of the cartilage, and the last observer (Schaffer) describes it as composed of thin walls of homogeneous material, in which there are no lines of separation, which form a simple honeycomb-structure, in the alveoli {130}of which the separate cells lie singly. These branchial cartilages are each surrounded by a layer of perichondrium, and in Fig. 55, A, I give a picture of a section of a portion of one of the bars.

Hence we see that structurally as well as topographically the branchial bars of Ammocoetes justify their claim to be considered as the origin of the vertebrate cartilaginous framework.

ON THE STRUCTURE OF THE MUCO-CARTILAGE IN AMMOCOETES.

We can, however, go further than this, and ask how this cartilage itself is formed in Ammocoetes? The answer is most definite, most instructive and suggestive, for in all cases this particular kind of cartilage is formed from, or at all events in, a peculiar fibrous tissue, which was called by Schneider "Schleim-Knorpel," or muco-cartilage, a tissue which is distinguishable from other connective tissues, not only by its structural peculiarities, but also by its strong affinity for all dyes which differentiate mucoid or chondro-mucoid substances.

This muco-cartilage is thus described by Schneider:--The perichondrium in Ammocoetes is not confined to the true cartilaginous structures, but extends itself in the form of thin plates in definite directions. Between these plates of perichondrium a peculiar tissue (Fig. 56)--the muco-cartilage--exists, consisting of fibrillæ, whose direction is mainly at right angles to the planes of the perichondrial plates, with star-shaped cells in among them, and with the spaces between the fibrillæ filled up with a semi-fluid mass.

{131}From this tissue all the primitive cartilages which resemble the branchial bars are formed, either by the invasion of chondroblasts from the surrounding perichondrium, or by the proliferation and encapsulation of the cells of the muco-cartilage itself.

This very distinctive tissue--the muco-cartilage--is of very great importance in all questions of the origin of the skeletal tissues. In all descriptions of the skeletal tissues it has been practically disregarded until recent years when, besides my own observations, its distribution has been mapped out by Schaffer. Thus Parker, in his well-known description of the skeleton of the marsipobranch fishes, does not even mention its existence. Its importance is shown by its absolute disappearance at transformation and its non-occurrence in any of the higher vertebrates. It is entirely confined to the head-region, and its distribution there is most suggestive, for, as will be described fully later on, it forms a skeleton which both in structure and position resembles very closely the head-shields of cephalaspidian fishes. At the present part of my argument its more immediate interest lies in the method of tracing this tissue. For this purpose I made use of the micro-chemical reaction of thionin, a dye which, as shown by Hoyer, stains all mucin-containing substances a bright purple. Schaffer made use of a corresponding basophil stain, hæmalum. When stained with thionin, the matrix, or ground-substance of the branchial cartilages as well as the matrix or semi-fluid substance in which the fibrils of the muco-cartilaginous cells are embedded take on a deep purple colour, while the fibrous material of the cranial walls and other connective tissue strands, such as the perichondrium, are coloured light blue. Muco-cartilage, then, may be described as a peculiar form of connective tissue which differs from other connective tissue not only in its appearance but in {132}its chemical composition, for unlike white fibrous tissue it contains a large amount of mucin, and this tissue is the forerunner of the earliest cartilaginous vertebrate skeleton, the branchial bars of Ammocoetes.

The conclusions to which we are led by the study of the structure, position, and mode of origin of these primitive cartilages of Ammocoetes may be thus summed up:--

1. The immediate ancestor of the vertebrate must have possessed a peculiar fibrous tissue--the ground-substance of which stained deep purple with thionin--in which cartilage arose.

2. The cartilage so formed was not like hyaline cartilage, but resembled in a striking manner parenchymatous cartilage.

3. This cartilage was situated partly in two axial longitudinal bands, partly as transverse bars, which supported the branchial apparatus.

THE PROSOMATIC OR BASI-CRANIAL SKELETON OF AMMOCOETES.

Before searching for any evidence of a similar tissue in any invertebrate group, it is advisable to consider the other portion of the cartilaginous skeleton of Ammocoetes, which consists of the trabeculæ, parachordals and auditory capsules--the basi-cranial skeleton--and is composed of hard, not soft cartilage.

This basi-cranial skeleton represented in Fig. 53, B, is confined to the region of the notochord, the cranial walls being composed entirely of a white fibrous membrane. It is separated at first entirely from the sub-chordal portion of the branchial basket-work, and is composed of a foremost part, the trabeculæ (_Tr._), and of a hindermost part, the parachordals (_Pr.ch._), which are characterized by the attachment on each side of the large auditory capsule (_Au._). In Ammocoetes the trabecular bars are continuous with the parachordals, the junction being marked by a small lateral projection on each side, which at transformation is seen to play an important part in the formation of the sub-ocular arch. The trabecular bar lies close against the notochord on each side up to its termination; it then bends away from the middle line and curves round until it meets its fellow on the opposite side, thus forming, as it were, the head of a racquet of which the notochord forms the splice in the handle. The strings of the racquet are represented by a thin membrane, in the centre of which the position of the infundibulum (_Inf._) of the {133}brain can be clearly seen. In an earlier stage of Ammocoetes the two trabecular horns do not meet, but are separated by connective tissue, which afterwards becomes cartilaginous.