the “ancient history” of bone

THE “ANCIENT HISTORY” OF BONE

Alfred Sherwood Romer Museum of Comparative Zoology, Harvard Unirwsily, Camlwidge, Mass.

In the study of human affairs, current problems are of major concern; but a knowledge of the history of man and human societies lends a breadth of vision which is of value in the solution of these problems. Just so in the study of bone. The main concerns are the problems encountered in the study of bony tissues as they occur in modern organisms; but a knowledge of the evolutionary history of these tissues is of value, as giving a broader perspective. I propose here to give a resume of modern concepts of the history of vertebrate skeletal tissues which, although imperfect, are far better-as well as radically different-from the ideas held in earlier periods of scientific discovery and investigation.

In the early decades of the century the story of the evolutionary development of vertebrate skeletal tissues appeared to be clear and simple. Most lowly of living vertebrates are the cyclostomes-the lampreys and hagiishes-in which neither jaws nor paired appendages are present. In them the skeleton is destitute of calcified tissues, and consists exclusively of cartilage. Mounting the scale to jawed fishes-gnathostomes rather than agnathous vertebrateswe find that a considerable fraction of such forms, including the sharks, skates, rays, and chimaeras, are likewise without bony skeletons. There are, to be sure, hard tissues in the form of teeth, skin denticles, and less commonly, spines; but dermal bones are absent, and the internal skeleton is formed exclusively of cartilage, although the cartilage is frequently of a calcified type. It is only when we come to the “higher” fishes that bone enters the picture. These fishes include the ray-finned forms (Actinopterygii), among which the teleosts are dominant today, the lungfishes (Dipnoi), and the almost extinct Crossopterygii. Here we find both an external sheathing of the body by bony scales, and replacement of internal cartilages by bony elements. It was thus not unreasonable that Goodrich, the outstanding morphologist of the times, divided the jawed fishes into two major groups, the Chondrichthyes, or cartilaginous fishes, and the “higher” bony fishes, the Osteichthyes (Good- rich, 1909). The assumed phylogenetic series ran : Agnatha (cyclostomes), lacking bone as well as jaws -P Chondrichthyes (sharks, skates, rays, chimaeras) with jaws but lacking bone + Osteichthyes, with bone finaHy developed.

These conclusions, based on the adult anatomy of modern fishes, appeared to be strongly corroborated by the embryological story of skeletal

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Romer: “Ancient History” of Bone 169

development in higher vertebrates. Dermal bones form, of course, directly; but in every instance internal skeletal structures are first formed in cartilage, and only as development proceeds does the transformation of these cartilages into bony elements take place. This would appear to be a perfect example of Haeckelian recapitulation, but even if (as has long been generally true) scientists are sceptical of the recapitulation idea, the ontogenetic picture harmonized well with the supposed phylogeny. There seemed no reason to disagree with the thesis that cartilage was the original skeletal tissue of vertebrates, and that bone appeared only at a late date in the history of fishes to augment and replace the cartilage.

There were, even half a century ago, some facts which, to be sure, did not fit into this seemingly clear and simple picture of vertebrate evolution. Even in the early studies of Agassiz on fossil fishes in the 1840’s, there had come to light among the oldest known fish faunas of the late Silurian and Devonian Old Red Sandstone a considerable number of fish-like vertebrates of obviously archaic structure, but with bony armor. Sommbviously quite primitive in structure, although presumably aberrant-were termed “ostracoderms” ; others, apparently rather more advanced if seemingly equally aberrant, were often lumped under the term “placoderms.” To have vertebrates with bony skeletons appear at such an early stage was somewhat disturbing; but, in general, the scientific difficulties of the situation were brushed aside by assuming that, for example, some of the placoderms were side-branches of the higher bony fishes; as for the ostracoderms, even such a keen student of fishes as Goodrich merely labeled them as “incertae sedis” and essentially forgot them.

The major turning point in our ideas of vertebrate skeletal history were the studies of Stensio, particularly his volume published in 1927 on the anatomy of ostracode:ms of the Cephalaspis group. Small ostracoderms of this sort had long been known, but our knowledge of their structure had been only of a most superficial sort. Into Stensios’s care came a suite of specimens from the early Devonian of Spitzbergen. These were studied by him in detail and with highly refined methods. A cephalaspid ostracoderm is characterized by a fish-like trunk and tail, encased in bony scales, with, anteriorly, a broad, flat crescentic ‘(cranial” structure. This “head” was, in much of his material, no larger than a postage stamp, but from it he was able to get a wealth of anatomical detail, partly by delicate dis- section with fine needles under a binocular, partly by grinding sections through the structure a t fractions of a millimeter and reconstructing the whole, enlarged, in a wax model. The “head,” it proved, included ventrally a much expanded series of gill-pouches; the animal appears (as might reasonably be expected of a primitive jawless vertebrate) to have been a filter-feeder, living like many lower chordates on food particles

170 Annals New York Academy of Sciences

strained out of a water current entering through the small mouth. In- ternally, there proves to have been an extensive consolidated head-plus-gill skeleton, partially ossified (the ossification appearing to be purely perichondral without endochrondral replacement-a point which I hope to discuss on some future occasion). Stensio was able, as a result of his dis- sections and reconstructions, to gain a very thorough knowledge of vascular, nervous, and sensory canals and cavities, of which the most interesting points were the presence of a single median nostril opening, placed high on the upper surface of the head, and an internal ear with only two semi- circular canals. These are characteristics not of vertebrates in general, but of cyclostomes, and of lampreys in particular.

This, of course, presented a new point of view on vertebrate history. The modern cyclostomes, with a purely cartilaginous skeleton, had been assumed to be very primitive in their absence of ossification. But here are forms among the oldest of known vertebrates which are not only primitive in general structural pattern, but; further, obviously allied to the lampreysand yet have a bony external skeleton and a fair degree of internal ossification as well.

The obvious answer was that our earlier ideas concerning skeletal evolution were wrong-that bone was an early rather than a late development among vertebrates. Stensio and other workers on lower vertebrates reviewed the field and noted that, on the whole, the later history of many fish groups showed the reverse of our former beliefs in that instead of an increase in bone in later types, there was a decrease-a tendency toward reduction toward or to a cartilaginous skeleton. Among the cephalaspids, later forms appear to have a feebler bony structure than the late Silurian and early Devonian forms. Other groups of ostracoderms have so far shown 110 evidence of endochondral ossification, but within these groups the’later Devonian members appear to show a lesser degree of dermal ossification than the earlier ones. Among the placoderms, too, there appears to have been a similar trend toward reduction. Certain placoderms of a more primitive type are completely encased in dermal armor, but in later forms this armor is mainly confined to the anterior part of the body. And as regards endochondral bones, early arthrodires of the placoderm group have a well ossified braincase, whereas the later members of this group are lacking in internal ossification. Furthermore, the &me trends toward reduction of ossification can be seen amongst higher fish groups. The earliest lungfishes appear to have had an ossified braincase (Lehmann and Westoll, 1952), but in later lungfishes the internal skeleton is almost entirely cartilaginous. The oldest crosvopterygians were highly ossified, in internal skeleton as well as dermal armor, but the sole survivor, Latimeria, is mainly cartilaginous in its “endochondral” elements (Millot

What does this mean?

Romer : “Ancient History’’ of Bone 171

and Anthony, 1958). Among the ray-finned fishes, the teleosts of today are highly ossified, but in the actinopterygian group the sturgeons and paddle-fishes, archaic members of the group in niost regards, have nearly completely lost the ossification of their internal skeleton, and (except for some rows of bony scutes in the sturgeons) have lost most of their dermal bone as well; with a slight further reduction, these living fishes, whose ancient palaeoniscoid ancestors were highly ossified, would be purely cartilaginous forms.

With these obvious tendencies toward bone reduction in many groups, what are we to think of the modern cyclostomes and sharks, forms which have no bone at all in their skeletons, and which were once thought to be truly primitive in this regard? We are led, inevitably, to the belief that their purely cartilaginous condition is not a truly primitive one, and that the absence of bone here is not an ancestral character, but one due to degeneration from bone-bearing ancestors. In agreement with this belief is the fact that in certain of the ostracodermsthe anaspids-which as regards general body proportions might well be ancestral to lampreys, most of the body armor has been lost, and all that is needed to turn an anaspid into a lamprey is some further loss of armor and the acquisition of a rasping tongue for preying on other fishes. As regards the sharks, it is probably significant that instead of being the oldest known group of fossil jawed vertebrates, as our former ideas of phylogeny would suggest, they are relatively late in appearance-far later than the supposedly “higher” Ostei- chthyes. Certain of the placoderms, with bony skeletons, appear to show, during the course of the Devoniaii, a reduction in the bony skeleton possessed by their early Devonian ancostors arid (although there is not universal agreement on this point) Stensiii and his school have marshalled evidence suggesting that the modern sharks, skates, and rays are placoderm descendants which have degenerated in their skeletal structure from an ancestral condition in which bone was present. Stensiii’s studies, backed up to a considerable degree by those of other students of early Vertebrates, such as Kiaer, Heintz, Westoll, and Watson, thus suggest that our earlier ideas of vertebrate skeletal evolution were the reverse of the truth- that instead of beginning with a purely cartilaginous skeleton and later gradually acquiring bone, the early vertebrates had a considerable degree of ossification which was followed in a majority of cases by a slump toward a cartilaginous condition. Bone is an ancient, rather than a relatively new, skeletal material in the history of Vertebrates.

Our knowledge of the earliest vertebrates is currently far from complete. We find a variety of ostracoderms in late Silurian deposits, and placoderms and early bony fishes close to the beginning of the succeeding Devonian period (the sharks, presumably degenerate, are considerably later in appear-


ance), A t the end of the Silurian and beginning of the Devonian, fishes were, thus, already highly diversified. Beyond this we know almost nothing except for fragmentary remains of a distinctive ostracoderm group from about the middle of the preceding Ordovician period. It is obvious, in consequence, that there was a considerable period of time preceding the late Silurian- period of perhaps close to a hundred million y e a d u r i n g which early vertebrates were developing but concerning which we know almost nothing.*

What was the earlier history of the vertebrate skeleton? At some time in early history the vertebrates arose from lower chordate ancestors in which there was little skeletal development of any sort, and certainly no bone. If one extrapolates backward, mentally, from the general “graph” of bone reduction in the history of most known fish groups in later periods, one may logically reach the conclusion that the ancestral vertebrates had developed a completely ossified skeleton, and that when we first get a reasonable picture of vertebrates in the late Silurian, we are looking a t forms in which degeneration was already far advanced. This, however, is an extreme position. The opposite point of view (cf, for example, White, 1946) is that when we first see late Silurian vertebrates they were just in the process of acquiring bone (presumably independently in several different lines). This is again an extreme position; it is difEcult to believe that if the vertebrates had just acquired bone at the time we first see them, they would have almost universally executed a right-about-face and immediately started to lose it again. We must wait, hopefully, for further evidence. A middle position, and a not unreasonable one, is the assumption that bone was present to a moderate degree in ancestral vertebrates as a group, but that bone was present mainly if not entirely in membrane form-dermal and perhaps perichondral to some degree as well. From this situation many forms tended toward loss, but others, mainly ancestral to bony fishes, tended to extend the degree of ossification toward that found today in teleosts and that characteristic of the ancestors of the well ossified land vertebrates.

If our modern ideas of vertebrate skeletal evolution are correct, why the prominence of cartilage in the embryological process? If we are not dealing with recapitulation, what is the point? The answer is so obvious that it is generally overlooked. Cartilage is, among vertebrates, essentially an embryonic adaptation. Cartilage-like materials are found here and there among the invertebrates; but even if no such material had been present in the ancestors of the vertebrates, it would have been necessary to invent

*My own belief-not shared by all my colleagues--is that them earliest vertebrata lived in fresh water, and that our lack of knowledge of them is due to the fact that we have few fresh water Ordovician and Silurian sedimentary deposits.

Romer : “Ancient History” of Bone 173

it, in order to achieve an orderly cmhryological development of a vertebrate which in the adult possesses a highly ossified skeleton (Romer, 1942).

The clue lies in the position and nature of vertebrate bony elements. One of the most elementary facts in the study of the skeleton is the classi- fication of bones into two types-membrane or dermal bones, which develop directly from mesenchyme condensations, and endochondral bones, in which a cartilaginous “model” of the element first forms, to be later re- placed, by an osseous structure. The two types differ strikingly in nature and position, for the most part. Dermal bones, present in mammals only in skull, jaws, and clavicles, are typically plate-like structures of simple form and without intimate connections with other organs. In consequence their development is without complication. Once a tiny rudiment of the plate is established, such a bone may grow indefinitely over the area it covers by accretions at its margins, and, since it usually has no major asso- ciation with other organs above or below, new layers may be readily added to inner and outer surfaces. It is thus possible for a superficial element of this sort to grow directly into bone without the aid of any other type of formative material.

Very different is the situation with regard to elements lying deeper in the body-as in braincase proper, backbone, and limbs. These are seldom simple plates; they generally have a complex structure with various processes which must be elaborated at an early stage of embryonic development; they are in general intimately connected with their skeletal neighbors in a complex architectural pattern which is established in the early embryo; still further, they tend to acquire, equally early, close relationships with elements of other organ systems, such as blood vessels, nerves, and muscles. How such an element is to grow from its tiny size in the embryo to adult volume presents a problem far more difficult of solution than in the case of a plate-like, dermal structure.

To take an obvious example: the human femur is well formed when the embryo is but a few centimeters long. Its general shape closely resembles that of the adult; it already has formed articulations with the girdle on the one hand, and with the tibia and fibula on the other; it further has already acquired a complex series of muscle insertions and has established close relations with adjacent nerves and blood vessels. The femur is at this stage only a few millimeters in length. To reach adult conditions it must increase its length a hundredfold, and its bulk perhaps ten thousand times, and yet do this without disturbing the relationships already established.

It is impossible to conceive of this growth being accomplished if the femur were formed of bone from the beginning. Bone is an unyielding material, incapable of expansion; it can grow or modify its proportions only by the addition of new layers on its surface or by the reverse process of absorption,


and these processes would inevitably disrupt the complex architectural patterns already developed. Obviously the only practicable method by which the ontogenetic development of a deep-lying bone can be accomplished is by making a tiny “model” in the early embryo out of some material of which the prime characteristic must be its ability to grow without disturbance of its surface. This quality is, of course, the most distinctive feature of cartilage. As a protective or supporting material it is much inferior to bone. But while cartilage may grow by superficial accretions, it contrasts with bone in its power of growth by internal expansion; its cells may divide and the daughter cells separate with the deposition of new materials between them. As such a cartilage grows, internal replacement of cartilage by bone may occur, additional bone may be added super- ficially to the less functionally important parts of the shaft, and, in mammals, accessory epiphysial bone centers may be lodged in the cartilage. At long last, with growth completed, the cartilages of mammalian elements have finished their task and bone takes over completely.

Thanks to the properties of cartilage, the whole job of growth can be done neatly and efficiently without any major disturbance of the surface of the element or of its relations to adjacent structures.

Cartilage, as mentioned previously, is apparently an ancient type of skeletal material. But, in the vertebrates, it is essentially an embryonic adaptation, and its prominence in the adult skeleton of many fishes is not a primitive feature but an evidence of neoteny.

What brought about its development at an early stage in vertebrate history? For higher terrestrial vertebrates its presence is a structural necessity. But, as we know, many fishes today do very well with little or no bone in their makeup.

One suggestion is that bone arose from physiological needs for. calcium storage (cf., for example, Westoll, 1942). But the topographic distribution of bone materials as we see them in the older vertebrates hardly lends support to such an assumption. If one were to imagine that bone arose in response to such a physiological need, the logical development would have been some sort of compact organ, designed for storage purposes, the position of which would have been of no importance except, one would imagine, it would have been ventrally situated, below the fish’s center of gravity. The bony skeleton of early vertebrates is no mere lump of storage tissue; it forms complex and characteristic patterns, spread mainly or entirely over the surface of the body in such a fashion that it seems obvious that in these forms (as in modern fishes) the body was top-heavy. Early bone, as modern bone, may have been physiologically important; but this function would appear to have been secondary rather than primary.

The late Homer Smith, whose studies on the kidney give the most con-

A final question-why bone?

This is, of course, far from the actual situation.

Romer : “Ancient History” of Bone 175

clusive proof that the early history of fishes centered in fresh water, has suggested (1939) that the major function of the bony armor was that of a protective covering that would reduce the tendency for dilution of body fluid salt content through osmosis. But if this had been the raison d’2tre of the dermal bone covering, nature did a poor job of construction. In almost every case the armor consists of three layers. The innermost is a layer of compact lamellar bone, impervious to osmotic action except for the presence of a few vascular canals. Splendid! But, external to this is a spongy layer, obviously highly vascular in nature. Further, although an external layer consists of dentine-like and enamel-like materials, this is penetrated by numerous pores which obviously supplied blood vessels to an external epithelium. As a bar to osmotic action, the dermal elements are the wrong way out-the most impervious layer is internal to vascular tissues.

The most reasonable answer is the most obvious one-that the dermal armor was, as it appears to be, armor for the animal. But armor against what? We customarily think of vertebrates as dominant in the animal kingdom. But we are, in the armored ostracoderms, dealing with the oldest of vertebrates, and there were no other vertebrates against whose predation they should be armed. That they ate one another does not sound reasonable; mutual cannibalism is hardly a satisfactory economic system. The answer appears to be that, in contrast to later times, the vertebrates were the underdogs. The predators against which they were shielded were invertebrates.

In locality after locality in which late Silurian and early Devonian fishes are found, we are dealing with fresh water deposits with very restricted faunas containing, as far as known, few animal types except primitive fishes and eurypterids. The latter are members of the arachnid class of arthropods, somewhat scorpion-like in general appearance, although of much larger size. They are frequently termed “marine scorpions,” but although all were obviously water dwellers, the Silurian and later members of this extinct group were, it is generally agreed, inhabitants of fresh waters. They were without question highly predaceous in habits, with effective biting mouth parts in addition to grasping claws. It is quite possible that soft-bodied invertebrates of other types were present, but the early fishes are almost the only forms preserved in the same localities with them, and seem to be their obvious prey. The eurypterids were, on the average, much larger than the inoffensive ostracoderms on which they appear to have preyed. The largest was some nine feet in length, and although this size was exceptional, the eurypterids were OH the whole much larger than the contemporary vertebrates, few of which were more than a few inches in length (Romer, 1933).

That the early fishes were the major prey of the eurypterids and that the


eurypterid menace was primarily responsible for the development of vertebrate bony armor seems to be borne out by the later history of the two groups. In later times, vertebrates tended to become much larger, to have become (particularly with the development of jaws and active feeding habits) faster swimmers and aggressors rather than inoffensive objects of aggression. With these changes, the vertebrates tended to free themselves from the eurypterid menace. And, in correlation, we find that the eurypterids rapidly dwindled into insignificance during the course of the De- vonian and became extinct before the close of the Paleozoic.

It thus seems highly probable that the bony skeleton without which the evolution of the higher vertebrates could never have taken place, owes its origin, close to half a billion years ago, to the threat of invertebrate predation on our feeble primitive fish ancestors.

References

1. GOODRICH, E. S. 1909. Vertebrata Craniata. First fascicle: Cyclostomes and fishes. A Treatise on Zoology, part IX. Lankester, Ed. Adam & Charles Black. London, England.

2. HEINTZ, A. 1935. How the fishes learned to swim. Smithson. Rept. lQS4: 223- 245.

3. LEHMANN, W. & T. S. WESTOLL. 1952. A primitive dipnoan fish from the Lower Devonian of Germany.

4. MILLOT, J. & J. ANTHONY. 1958. Anatomie de Latimeria chalumnae. Tome I. Squelette, muscles et formations de soutien. Paris. Centie National de la Recherche scientifique. Pp. 1-122.

5. ROMER, A. S. 1933. Eurypterid influence on vertebrate history. Science. 78: 114-117.

6. ROMER. A. S. 1942. Cartilage an embryonic adaptation. Amer. Nat. 76:

Proc. Roy. SOC. London, B. 140: 403-421.

~ 394-404. 7. SMITE, H. W. 1939. Studies in the physiology of the kidney. Univ. Kansas,

I

Porter Lecture Series. 4: 1- 106.

Pt. I: Family Cephalaepidae. Skr. Svalb. Nordish. 1%: 1-391. 8. STENSI~, E. A. 1927. The Downtonian and Devonian vertebrates of Spitzbergen.

9. WESTOLL, T. S. 1942. The earliest Panzergruppen. Aberdeen Univ. Rev.

1946. Jamytius kwwoodi, a new chordate from the Silurian of Pp. 114-122.

10. WHITE, E. I. Lanarkehire. Geol. Mag. 88: 89-97.

the “ancient history” of bone

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