Origin of Vertebrates/Chapter VI
CHAPTER VI
THE EVIDENCE OF THE OLFACTORY APPARATUS
Fishes divided into Amphirhinæ and Monorhinæ.—Nasal tube of the lamprey.—Its termination at the infundibulum.—The olfactory organs of the scorpion group.—The camerostome.—Its formation as a tube.—Its derivation from a pair of antennæ.—Its termination at the true mouth.—Comparison with the olfactory tube of Ammocœtes.—Origin of the nasal tube of Ammocœtes from the tube of the hypophysis.—Direct comparison of the hypophysial tube with the olfactory tube of the scorpion group—Summary.
In the last chapter I finished the evidence given by the consideration of the mesosomatic or opisthotic nerves, and the segments they supplied. The evidence is strongly in accordance with that of previous chapters, and not only confirms the conclusion that vertebrates arose from some member of the Palæostraca, but helps still further to delimit the nature of that member. It is almost startling to see how the hypothesis put forward in the second chapter, suggested by the consideration of the nature of the vertebrate central nervous system and of the geological record, has received stronger and stronger confirmation from the consideration of the vertebrate optic apparatus, the vertebrate skeleton, the respiratory apparatus, and, finally, the thyroid gland. All fit naturally into a harmonious whole, and give a feeling of confidence that a similar harmony will be found upon consideration of the rest of the vertebrate organs.
Following naturally upon the segments supplied by the opisthotic (mesosomatic) cranial nerves, we ought to consider now the segments supplied by the pro-otic (prosomatic) cranial nerves, i.e. the segments belonging to the trigeminal nerve-group in the vertebrate, and in the invertebrate the segments of the prosoma with their characteristic appendages. There are, however, in all vertebrates in this foremost cranial region, in addition to the optic nerves, two other well-marked nerves of special sense, the olfactory and the auditory. Of these, the former are in the same class as the optic nerves, for they arise in the vertebrate from the supra-infundibular nerve-mass, and in the invertebrate from the supra-œsophageal ganglia. The latter arise in the vertebrate from the infra-infundibular nerve-mass, and, as the name implies, are situated in the region where the pro-otic nerves are contiguous to the opisthotic, i.e. at the junction of the prosomatic and mesosomatic nerve-regions.
The chapter dealing with the evidence given by the olfactory nerves and the olfactory apparatus ought logically to have followed immediately upon the one dealing with the optic apparatus, seeing that both these special sense-nerves belong to the supra-infundibular segments in the vertebrate and to the supra-œsophageal in the invertebrate.
I did not deal with them in that logical sequence because it was necessary for their understanding to introduce first the conception of modified appendages as important factors in any consideration of vertebrate segments; a conception which followed naturally after the evidence afforded by the skeleton in Chapter III., and by the branchial segments in Chapter IV. So, too, now, although the discussion of the prosomatic segmentation ought logically to follow immediately on that of the mesosomatic segmentation, I have determined to devote this chapter to the evidence of the olfactory organs, because the arguments as to the segments belonging to the trigeminal nerve-group are so much easier to understand if the position of the olfactory apparatus is first made clear.
In all vertebrates the nose is double and opens into the pharynx, until we descend to the fishes, where the whole group Pisces has been divided into two subsidiary groups, Monorhinæ and Amphirhinæ, according as they possess a median unpaired olfactory opening, or a paired opening. The Monorhinæ include only the Cyclostomata—the lampreys and hag-fishes.
In the lampreys the single olfactory tube ends blindly, while in the hag-fishes it opens into the pharynx. In the lamprey, both in Petromyzon and Ammocœtes, the opening of this nasal tube is a conspicuous object on the dorsal surface of the head in front of the transparent spot which indicates the position of the right median eye. It is especially significant, as showing the primitive nature of this median olfactory passage, that a perfectly similar opening in the same position is always found in the dorsal head-shields of all the Cephalaspidæ and Tremataspidæ, as will be explained more fully in Chapter X.
All the evidence points to the conclusion that the olfactory apparatus of the vertebrate originated as a single median tube, containing the special olfactory sense-epithelium, which, although median and single, was innervated by the olfactory nerve of each side. The external opening of this tube in the lamprey is dorsal. How does it terminate ventrally?
The ventral termination of this tube is most instructive and suggestive. It terminates blindly at the very spot where the infundibular tube terminates blindly and the notochord ends. After transformation, when the Ammocœte becomes the Petromyzon, the tube still ends blindly, and does not open into the pharynx as in Myxine; it, however, no longer terminates at the infundibulum, but extends beyond it towards the pharynx.
This position of the nasal tube suggests that it may originally have opened into the tube of the central nervous system by way of the infundibular tube. This suggestion is greatly enhanced in value by the fact that in the larval Amphioxus the tube of the central nervous system is open to the exterior, its opening being known as the anterior neuropore, and this anterior neuropore is situated at the base of a pit, known as the olfactory pit because it is supposed to represent the olfactory organ of other fishes.
Following the same lines of argument as in previous chapters, this suggestion indicates that the special olfactory organs of the invertebrate ancestor of the vertebrates consisted of a single median olfactory tube or passage, which led directly into the œsophagus and was innervated, though single and median, by a pair of olfactory nerves which arose from the supra-œsophageal ganglia. Let us see what is the nature of the olfactory organs among arthropods, and whether such a suggestion possesses any probability.
The Olfactory Organs of the Scorpion Group.
At first sight the answer appears to be distinctly adverse, for it is well known that in all the Insecta, Crustacea, and the large majority of Arthropoda, the first pair of antennæ, often called the antennules, are olfactory in function, and these are free-moving, bilaterally situated, independent appendages. Still, even here there is the striking fact that the nerves of these olfactory organs always arise from the supra-œsophageal ganglia, although those to the second pair of antennæ arise from the infra-œsophageal ganglia, just as the olfactory nerves of the vertebrate arise from the supra-infundibular brain-mass. Not only is there this similarity of position, but also a similarity of structure in the olfactive lobes of the brain itself of so striking a character as to cause Bellonci to sum up his investigations as follows:—
"The structure and connections of the olfactive lobes present the same fundamental plan in the higher arthropods and in the vertebrates. In the one, as in the other, the olfactory fibres form, with the connecting fibres of the olfactory lobes, a fine meshwork, which, consisting as it does of separate groups, may each one be called an olfactory glomerulus."
He attributes this remarkable resemblance to a physiological necessity that similarity of function necessitates similarity of structure, for he considers it out of the question to suppose any near relationship between arthropods and vertebrates.
Truly an interesting remark, with the one fallacy that relationship is out of the question.
The evidence so far has consistently pointed to some member of the palæostracan group as the ancestor of the vertebrates—a group which had affinities both to the crustaceans and the arachnids; indeed, many of its members resembled scorpions much more than they resemble crustaceans. The olfactory organs of the scorpions and their allies are, therefore, more likely than any others to give a clue to the position of the desired olfactory organs. In these animals and their allies paired olfactory antennæ are not present, either in the living land-forms or the extinct sea-scorpions, for all the antennæ-like, frequently chelate, appendages seen in Pterygotus, etc. (Fig. 8), represent the cheliceræ, and correspond, therefore, to the second pair of antennæ in the crustaceans.
What, then, represents the olfactory antennæ in the scorpions? The answer to this question has been given by Croneberg, and very striking it is. The two olfactory antennæ of the crustacean have combined together to form a hollow tube at the base of which the mouth of the animal is situated, so that the food passes along this olfactory passage before it reaches the mouth. This organ is often called after Latreille, the camerostome, sometimes the rostrum; it is naturally median in position and appears, therefore, to be an unpaired organ; its paired character is, of course, evident enough, for it is innervated by a pair of nerves, and these nerves, as ought to be the case, arise from the supra-œsophageal ganglia. In Galeodes it is a conspicuously paired antennæ-like organ (Fig. 94).
Croneberg has also shown that this rostrum, or camerostome, arises embryologically as a pair of appendages similar to the other appendages. This last observation of Croneberg has been confirmed by Brauer in 1894, who describes the origin of the upper lip, as he calls it, in very similar terms, without, however, referring to Croneberg's paper. Croneberg further shows that this foremost pair of antennæ not only forms the so-called upper lip or camerostome, but also a lower lip, for from the basal part of the camerostome there projects on each side of the pharynx a dependent accessory portion, which in some cases fuses in the middle line, and forms, as it were, a lower lip. The entosclerite belonging to this dependent portion is apparently the post-oral entosclerite of Lankester and Miss Beck.
Fig. 94.—Dorsal View of Brain and Camerostome of Galeodes.
At the base of the tubular passage formed by this modified first pair of antennæ the true mouth is found opening directly into the dilated pharynx, the muscles of which enable the act of suction to be carried out. The narrow œsophagus leads out from the pharynx and is completely surrounded by the supra- and infra-œsophageal nerve masses.
Huxley also describes the mouth of the scorpion in precisely the same position (cf. o, Fig. 96).
In order to convey to my readers the antennæ-like character of the camerostome in Galeodes (Fig. 101), and its position, I give a figure (Fig. 94) of the organ from its dorsal aspect, after removal of the cheliceræ and their muscles. A side view of the same organ is given in Fig. 95 to show the feathered termination of the camerostome, and the position of the dependent accessory portion (l.l.) (Croneberg's 'untere Anhang') with its single long antenna-like feather. In both figures the alimentary canal (al.) is seen issuing from the conjoined supra- and infra-œsophageal mass.
As is seen in the figures, the bilateral character of the rostrum, as Croneberg calls it, is apparent not only in its feathered extremity but also in its chitinous covering, the softer median dorsal part (left white in figure) being bounded by two lateral plates of hard chitin, which meet in the middle line near the extremity of the organ. In all the members of the scorpion group, as is clearly shown in Croneberg's figures, the rostrum or camerostome is built up on the same plan as in Galeodes, though the antenna-like character may not be so evident.
Fig. 95.—Lateral View of Brain and Camerostome of Galeodes.
gl. supr. œs., supra-œsophageal ganglion; gl. infr. œs., infra-œsophageal ganglion. The rest of the lettering same as in Fig. 94.
When we consider that the first pair of antennæ in the crustaceans are olfactory in function, Croneberg's observations amount to this—
In the arachnids and their allies the first pair of antennæ form a pre-oral passage or tube, olfactory in function; the small mouth, which opens directly into the pharynx, being situated at the end of this olfactory passage.
Croneberg's observations and conclusions are distinctly of very great importance in bringing the arachnids into line with the crustaceans, and it is therefore most surprising that they are absolutely ignored by Lankester and Miss Beck in their paper published in 1883, in which Latreille only is mentioned with respect to this organ, and his term "camerostome," or upper lip, is used throughout, in accordance with the terminology in Lankester's previous paper. That this organ is not only a movable lip or tongue, but essentially a sense-organ, almost certainly of smell and taste, as follows from Croneberg's conclusions, is shown by the series of sections which I have made through a number of young Thelyphonus (Fig. 102).
Fig. 96.—Median Sagittal Section through a Young Thelyphonus.
I give in Fig. 96 a sagittal median section through the head-end of the animal, which shows clearly the nature of Croneberg's conception. At the front end of the body is seen the median eye (ce.), o is the mouth, Ph. the pharynx, œs. the narrow œsophagus, compressed between the supra-œsophageal (supr. œs.) and infra-œsophageal (infr. œs.) brain mass, which opens into the large alimentary canal (Al.); Olf. pass. is the olfactory passage to the mouth, lined with thick-set, very fine hairs, which spring from the hypostome (Hyp.) as well as from the large conspicuous camerostome (Cam.), which limits this tube anteriorly. The space between the camerostome and the median eye is filled up by the massive cheliceræ, which are not shown in this section, as they begin to appear in the sections on each side of the median one. The muscles of the pharynx and the muscles of the camerostome are attached to the pre-oral entosclerite (pr. ent.). The post-oral entosclerite is shown in section as post. ent. The dorsal blood-vessel, or heart, is indicated at H.
In Fig. 97 I give a transverse section through another specimen of the same litter, to show the nature of this olfactory tube when cut across. Both sections show most clearly that we are dealing here with an elaborate sense-organ, the surface of which is partly covered with very fine long hairs, partly, as is seen in the figure, is composed of long, separate, closely-set sense-rods (bat.), well protected by the long hairs which project on every side in front of them, which recall to mind Bellonci's figure of the 'batonnets olfactives' on the antennæ of Sphæroma. Finally, we have the observation of Blanchard quoted by Huxley, to the effect that this camerostome is innervated by nerves from the supra-œsophageal ganglia which are clearly bilateral, seeing that they arise from the ganglion on each side and then unite to pass into the camerostome; in other words, paired olfactory nerves from the supra-œsophageal ganglia.
These facts demonstrate with wonderful clearness that in one group of the Arthropoda the olfactory antennæ have been so modified as to form an olfactory tube or passage, which leads directly into the mouth and so to the œsophagus of the animal, and, strikingly enough, this group, the Arachnida, is the very one to which the scorpions belong.
If for any cause the mouth o in Fig. 96 were to be closed, then the olfactory tube (olf. pass.) might still remain, owing to its importance as the organ of smell, and the olfactory tube would terminate blindly at the very spot where the corresponding tube does terminate in the vertebrate, according to the theory put forward in this book.
The Olfactory Tube of Ammocœtes.
In all cases where there is similarity of topographical position in the organs of the vertebrate and arthropod we may expect also to find similarity of structure. At first sight it would appear as though such similarity fails us here, for a cross-section of the olfactory tube in Petromyzon represents an elaborate organ such as is shown in Fig. 98, very different in appearance to the section across the olfactory passage of a young Thelyphonus given in Fig. 97.
Fig. 97.—Transverse Section through the Olfactory Passage of a Young Thelyphonus.
1 and 2, sections of first and second appendages.
Fig. 98.—Transverse Section through the Olfactory Passage of Petromyzon.
cart., nasal cartilage.
As is seen, it is difficult to see any connection between these folds of olfactory epithelium and the simple tube of the scorpion. But in the nose, as in all other parts of the head-region of the lamprey, remarkable changes take place at transformation, and examination of the same tube in Ammocœtes demonstrates that the elaborate structure of the adult olfactory organ is actually derived from a much simpler form of organ, represented in Fig. 99. Here, in Ammocœtes, the section is no longer strikingly different from that of the Thelyphonus organ, but, instead, most strikingly similar to it. Thus, again, it is shown that this larval form of the lamprey gives more valuable information as to vertebrate ancestry than all the rest of the vertebrates put together.
Fig. 99.—Transverse Section through the Olfactory Passage of Ammocœtes.
cart., nasal cartilage.
Still, even now the similarity between the two organs is not complete, for the tube in the lamprey opens on to the exterior on the dorsal surface of the head, while in the scorpion tribe it is situated ventrally, being the passage to the mouth and alimentary canal. In accordance with this there is no sign of any opening on the dorsal carapace of any of the extinct sea-scorpions or of the living land-scorpions, such as is so universally found in the cephalaspids, tremataspids, and lampreys. Here is a discrepancy of an apparently serious character, yet so wonderfully does the development of the individual recapitulate the development of the race, that this very discrepancy becomes converted into a triumphant vindication of the correctness of the theory advocated in this book, as soon as we turn our attention to the development of this nasal tube in the lamprey.
We must always remember not only the great importance of a larval stage for the unriddling of problems of ancestry, but also the great advantage of being able to follow more favourably any clues as to past history afforded by the development of the larva itself, owing to the greater slowness in the development of the larva than of the embryo. Such a clue is especially well marked in the course of development of Ammocœtes according to Kupffer's researches, for he finds that when the young Ammocœtes is from 5 to 7 mm. in length, some time after it has left the egg, when it is living a free larval life, a remarkable series of changes takes place with considerable rapidity, so that we may regard the transformation which takes place at this stage, as in some degree comparable with the great transformation which occurs when the Ammocœtes becomes a Petromyzon.
All the evidence emphasizes the fact that the latter transformation indicates the passage from a lower into a higher form of vertebrate, and is to be interpreted phylogenetically as an indication of the passage from the Cephalaspidian towards the Dipnoan style of fish. If, then, the former transformation is of the same character, it would indicate the passage from the Palæostracan to the Cephalaspid.
What is the nature of this transformation process as described by Kupffer?
It is characterized by two most important events. In the first place, up to this time the oral chamber has been cut off from the respiratory chamber by a septum—the velum—so that no food could pass from the mouth to the alimentary canal. At this stage the septum is broken through, the oral chamber communicates with the respiratory chamber, and the velar folds of the more adult Ammocœtes are left as the remains of the original septum. The other striking change is the growth of the upper lip, by which the orifice of the nasal tube is transferred from a ventral to a dorsal position. Fig. 100, taken from Kupffer's paper, represents a sagittal section through an Ammocœtes 4 mm. long; l.l. is the lower lip, u.l. the upper lip, and, as is seen, the short oral chamber is closed by the septum, vel. Opening ventrally is a tube called the tube of the hypophysis, Hy., which extends close up to the termination of the infundibulum. On the anterior surface of this tube is the projection called by Kupffer the olfactory plakode. At this stage the upper lip grows with great rapidity and thickens considerably, thus forcing the opening of the hypophysial tube more and more dorsalwards, until at last, in the full-grown Ammocœtes, it becomes the dorsal opening of the nasal tube, as already described. Here, then, in the hypophysial tube we have the original position of the olfactory tube of the vertebrate ancestor, and it is significant, as showing the importance of this organ, to find that such a hypophysial tube is characteristic of the embryological development of every vertebrate, whatever may be the ultimate form of the external nasal orifices.
The single median position of the olfactory organ in the Cyclostomata, in contradistinction to its paired character in the rest of the vertebrates, has always been a stumbling-block in the way of those who desired to consider the Cyclostomata as degenerated Selachians, for the origin of the olfactory protuberance, as a single median plakode, seemed to indicate that the nose arose as a single organ and not as a paired organ.
Fig. 100.—Ganglia of the Cranial Nerves of an Ammocœtes, 4 mm. in length, projected on to the Median Plane. (After Kupffer.)
On the other hand, the two olfactory nerves of Ammocœtes compare absolutely with the olfactory nerves of other vertebrates, and force one to the conclusion that this median organ of Ammocœtes arose from a pair of bilateral organs, which have fused in the middle line.
Fig. 101.—Galeodes. (From the Royal Natural History.)
The comparison of this olfactory organ with the camerostome gives a satisfactory reason for its appearance in the lowest vertebrates as an unpaired median organ; equally so, the history of the camerostome itself supplies the reason why the olfactory nerves are double, why the organ is in reality a paired organ and not a single median one. Thus, in a sense, the grouping of the fishes into Monorhinæ and Amphirhinæ has not much meaning, seeing that the olfactory organ is in all cases double.
Fig. 102.—Thelyphonus. (From the Royal Natural History.)
The evidence of the olfactory organs in the vertebrate not only confirms, in a most striking manner, the theory of the origin of the vertebrate from the Palæostracan, but points indubitably to an origin from a scorpion-like rather than a crustacean-like stock. To complete the evidence, it ought to be shown that the ancient sea-scorpions did possess an olfactory passage similar to the modern land-scorpions. The evidence on this question will come best in the next chapter, where I propose to deal with the prosomatic appendages of the Palæostracan group.
Summary.
The vertebrate olfactory apparatus commences as a single median tube which terminates dorsally in the lamprey, and is supplied by the two olfactory nerves which arise from the supra-infundibular portion of the brain. It is a long, tapering tube which passes ventrally and terminates blindly at the infundibulum in Ammocœtes. The dorsal position of the nasal opening is not the original one, but is brought about by the growth of the upper lip. The nasal tube originally opened ventrally, and was at that period of development known as the tube of the hypophysis.
The evidence of Ammocœtes thus goes to show that the olfactory apparatus started as an olfactory tube on the ventral side of the animal, which led directly up to, and probably into, the œsophagus of the original alimentary canal of the palæostracan ancestor.
Strikingly enough, although in the crustaceans the first pair of antennæ form the olfactory organs, no such free antennæ are found in the arachnids, but they have amalgamated to form a tube or olfactory passage, which leads directly into the mouth and œsophagus of the animal.
This olfactory passage is very conspicuous in all members of the scorpion group, and, like the olfactory tube of the vertebrate, is innervated by a pair of nerves, which resemble those supplying the first pair of antennæ in crustaceans as to their origin from the supra-œsophageal ganglia.
This nasal passage, or tube of the hypophysis, corresponds in structure and in position most closely with the olfactory tube of the scorpion group, the only difference being that in the latter case it opens directly into the œsophagus, while in the former, owing to the closure of the old mouth, it cannot open into the infundibulum.
The evidence of the olfactory apparatus, combined with that of the optic apparatus, is most interesting, for, whereas the former points indubitably to an ancestor having scorpion-like affinities, the structure of the lateral eyes points distinctly to crustacean, as well as arachnid, affinities.
Taking the two together the evidence is extraordinarily strong that the vertebrate arose from a member of the palæostracan group with marked scorpion-like affinities.