The Evolution and Development of the Dens of the Mammalian Axis FARISH A. JENKINS, JR. Department of Anatomy, College of Physicians and Surgeons, Columbia University, N e w Yorlz, N e w Yorlz 10032 ABSTRACT Certain members of the extinct reptilian group from which mammals evolved possessed both a dens and a n atlas body. Available paleontologic evidence supports the conclusion that the dens evolved as an addition to the atlas body. Therefore, the dens is not homologous with the atlas body as is generally claimed on the basis of supposed developmental evidence. The atlas body is large in the most primitive of living mammaIs, the monotremes, which also possess a dens of typicaI mammalian proportions. In metatherian and most eutherian mammals, both a dens and an atlas body remnant of variable size are present. The development of the dens in the Virginia opossum, Didelphis marsupialis, confirms the fact that the dens arises from, but does not replace, the a t h body anlage. The dens evolved as a functional replacement of the atlanto-axial articular processes which were lost when the mammalian atlanto-axial joint became specialized for rotational movement. The dens of the mammalian axis is a bony, peg-like process which projects craniad into the atlas ring. The dens is present in all living members of all orders of mammals except Cetacea (whales, dolphins). The loss of the dens in most modern cetaceans is secondary, for it is clearly present in fossil representatives of this order which lived during early Tertiary times (Kellogg, ’36). A few modern cetaceans possess a vestigial dens. The origin of the dens, both developmentally and phylogenetically, is often expressed in terms of homology with the atlas body of primitive tetrapods. Textbooks of human anatomy usually state simply that the dens represents “...the (Trotter displaced body of the atlas.. .the lost body of and Peterson, ’66) or the atlas. , (Lockhart et al., ’65). Other texts imply or explicitly state that embryologic evidence establishes that the dens is the homologue of the atlas body (e.g., Sisson and Grossman, ’53; Young, ’57; Romer, ’62; Crouch, ’65). The concept of an atlas body-dens homology is one of the oldest in comparative anatomy. Cuvier (1835) probably first expressed the general idea, but he merely employed the tern “analogue” (not homology). It is doubtful whether Cuvier recognized the concept of homology as later proposed by Owen, for homology in its strictest sense implies evolutionary continuity and Cuvier did not believe in .” ANAT. REC., 164: 173-184. “. . .” evolution. Rathke’s (1839) statement, that “Der Korper des Atlas aber verschmilzt mit dem Epistropheus, und macht dann den Processus odontoideus desselben ans,” is perhaps the first positive statement of the equivalency of the dens and atlas body. This statement was made specscally with regard to the axis of a snake (Coluber natrix), and the mammalian condition was not discussed; but it is obvious that to Rathke, at least, the term odontoid process could signify the atlas body of reptiles as well as the dens of mammals (from which it presumably derived its name). Whether intentional or not, these terms were already synonymous. Bergmann (1845) subsequently compared the atlas and axis in mammals, reptiles and birds, and was probably the first to make an unequivocal claim that the so-called 0s odontoideum of mammals represents the atlas body of lower tetrapods. The concept was fully accepted and promulgated by Owen (1854), Robin (1864) and other anatomists who subsequently undertook a comparative study of the atlas-axis complex. Firsthand information on the development of the dens is limited. Such studies as are available do not necessarily support the supposed strict homology between the dens and atlas centrum. Macalister’s (1894) findings are typical; he states that Received Dec. 2, ’68. Accepted Jan. 21. ’69. 173 174 FARISH A. JENKINS, JR. the cartilaginous dens forms from the “perichondral body’’ of the atlas, i.e., from material in a position expected of an atlas body. But there is no statement that the dens is the homologue of the atlas body. Superficially, at least, the developmental processes of the mammalian dens and the reptilian atlas centrum are sufficiently similar as to suggest strict homology. Both are developed through sclerotomic resegmentation of the first and second cervical sclerotomes and by addition of material from a “pro-atlantal” sclerotomite. During sclerotomic resegmentation in amniotes, the caudal sclerotomite of the fist cervical sclerotome combines with the cranial sclerotomite of the second cervical sclerotome, thus forming the anlage of the atlantal arches and body. The cranial sclerotomite of the first cervical sclerotome does not combine with another (caudal) sclerotomite, but it left alone, so to speak, to follow a variety of developmental courses. In mammals, one such course was thought by early workers to lead to the formation of the anterior chondrification center of the dens (Goodrich, ’30; Cave, ’38). The contribution of this socalled “pro-atlantal” sclerotomite in forming the tip of the dens has since been confirmed in several mammals (Dawes, ’30; Sensenig, ’43), including man (Sensenig, ’57). In reptiles, the anterior half of the atlas body is also formed by a “proatlantal” sclerotomite, i.e., the cranial half of the first cervical sclerotome (Hayek, ’24). The dorsal half of this ‘‘pro-atlantal” sclerotomite is almost certainly the anlage of the proatlas ossicle in those reptiles which retain this primitive feature. In mammals a proatlas does not develop; instead, the arch anlage of the “pro-atlantal” sclerotomite (as opposed to the body anlage which comprises the tip of the dens) enters into the formation of the cranial edge of the atlas ring (cf. Sensenig, ’43). Despite the apparent simple developmental history of the dens, opinions are diverse as to the composition of the dens in terms of the separate parts of the primitive atlas. For example, Romer (’62) states that the dens also includes the intercentrum of the atlas, while Lessertisseur and Saban (’67)admit the additional pos- sibility that the axial intercentrum may be completely lost. Miller et al. (’64) claim .is morphologthat in the dog the dens ically the caudal part of the body of the atlas,. ,”, implying thereby that a cranial part is not accounted for or is lost. The paradox of the developmental evidence to date is that although it seems to justify a dens-atlas body homology, it does not precisely delineate the composition of the dens or the morphological division between the axis body and atlas body. Furthermore, the developmental evidence is clearly insufficient as a guide to the phylogenetic history of the dens which yields a more precise account of its characteristic shape and relations. The present study attempts to summarize and to correlate the developmental, evolutionary and functional aspects of this important mammalian structure. The critical question is whether the dens, at any time from its initial differentiation through its completed development (both in the embryological and evolutionary sense), can be regarded as homologous with the atlas body of reptiles and other primitive tetrapods. Separate development of the dens could possibly be construed as evidence for its homology with the primitive atlas body. Conversely, its development as a process arising from a post-dens oss& cation would support the hypothesis that the dens arises as an addition to the atlas body, and is not homologous with it. “. . MATERIALS AND METHODS Fossil skeletal material pertaining to the evolution of the dens among cynodont therapsids (advanced mammal-like reptiles from which mammals probably evolved) was studied with the aid of a dissecting microscope. This material includes : Thrinaxodon Ziorhinus, British Museum of Natural History nos. R. 511, R. 511a, and 3731; Galesaurus planiceps, University Museum of Zoology (Cambridge, England) no. R. 2721; and two specimens referred to as Diademodon sp., D.M.S. Watson Collection nos. R. 204 and R. 205 (housed in the University Museum of Zoology, Cambridge, England). Skeletal material pertaining to the development of the dens among representatives of the orders of modern mammals was studied by gross ex- THE MAMMALIAN DENS amination; this material is cited below by museum number with the following abbreviations : AMNH, American Museum of Natural History; YPMOC,Osteological Collection of Peabody Museum, Yale University. The early development of the dens in the opossum, Didelphis marsupialis, was studied by light microscopic examination of sagittal sections through the atlas and axis of a 20 day and 25 day post partum pouch young. Sections of the 20 day old individual were bormwed from the Wistar Institute Collection, Serial Catalogue No. 17683. The atlas and axis of the 25 day old individual were serially sectioned at 7 CI and stained with hematoxylin and triosin. The skeleton of a second 25 day old individual was stained with alizarin red S and studied intact after the soft tissues had been cleared. 175 and thus the vertebral arch halves are capable of movement on the atlas body. In addition, a pair of proatlas ossicles link each atlas arch half with the occiput (pa, fig. IB). The structural evolution of the dens is clarified by first reviewing the paleontological evidence. In pelycosaurs the basic plan of the atlas-axis complex, as noted above, is essentially reptilian. The atlas body is comparable in size to other cervical bodies, although its anteroposterior length is shortened. Vertebral bodies in pelycosaurs are amphicoelous, i.e., possess a deep, funnel-shaped concavity or fossa at each end (Romer and Price, ’40). The apex of each funnel-shaped fossa is directed toward the center of the body. The apices of each pair of fossae communicate by a small foramen through the middle of the vertebral body. Thus each body enOBSERVATIONS closes an hour glass shaped space which In adult mammals the atlas-axis com- is open at either end. In embryonic plex usually consists of only two bones - modern reptiles, the vertebral body enthe atlas and axis vertebrae. In living closes a similar “space” which is occupied reptiles the atlas-axis complex may con- by the notochord. The embryonic cartilage sist of as many as eight separate bones. is first laid down around the notochord That the reptilian condition is phyloge- near the middle of the developing body; netically antecedent to the mammalian ar- subsequent enlargement of notochord is rangement is demonstrated by the fossil therefore restricted at this point, but is alremains of some of the reptilian ancestors lowed to continue towards either end. of mammals, i.e., pelycosaurs (Romer and Thus in late embryonic stages the notoPrice, ’40). In pelycosaurs and in rela- chord is constricted intravertebrally and tively generalized living reptiles, there are expanded intervertebrally. The differential two bodies for each vertebral segment. growth of the notochord is recorded in the The anterior of the two bodies is wedge- shape of the space within each vertebral shaped and is smaller than the other; it is body. The initial site of pericordal choncommonly referred to as the intercentrum drification becomes the foramen; subseor hypocentrum (ic, fig. 1B). The second quent chondrification around the notobody lies posteriorly and is spool-shaped; chord which is increasing in diameter reit is usually referred to as the centrum or sults in the two funnel-shaped fossae pleurocentrum and is homologous with within the body. Among modern reptiles, the body of the mammalian vertebra. In the amphicoelous type of vertebral body the following discussion, the anterior of (with a communicating foramen) persists the two bodies will be referred to as the into adult life only in geckos, Sphmodon, intercentrum, while the posterior will be and in the trunk vertebrae of turtles; tissue designated (following common anatomical derived from the degenerated notochord, usage) as the body or corpus. In addition often fibrous, occupies the fossae and the to an intercentrum and body, the atlas of center of the intervertebral discs (Romer, reptiles typically has an incomplete verte- ’56). In the folIowing discussion, the funbral arch. The two halves of the arch do nel-shaped fossae of amphiocoelous vertenot synostose sagittally above the vertebral brae will be referred to as notochordal canal. Moreover, the articulation of each fossae as a reminder of both the developpedicle with the atlas body is diarthrodial, mental process and the enveloped tissues. 176 FARISH A. JENKINS, JR. On the anterior aspect of the atlas body in pelycosaurs, the notochordal fossa is shallower and smaller in diameter than in other centra (nf, fig. 1C). Moreover, instead of occurring in the center of the anterior aspect, it is located slightly above center. This fossa is apposed by a similarly structured fossa on the occipital condyle (nf, fig. 1A). The eccentric position and reduced size of the anterior notochordal fossa is the most salient modification of the atlas body which is otherwise typically reptilian. A dens is certainly not present at this phylogenetic stage. The next stage in atlas-axis evolution is found among cynodont therapsids, a group of advanced mammal-like reptiles from which mammals probably arose ( c f . Crompton and Jenkins, '68). In cynodonts all the separate elements of the pelycosaur atlas-axis are retained (fig. lE), but with several modifications. Among the most significant of these is the loss of all vestiges of the primitive notochordal fossa on the anterior aspect of the atlas body. In place of the fossa, and slightly above it, occurs a small protuberance which may be interpreted as an incipient dens, or odontoid process (d, fig. 1F). If this interpretation is correct, namely, that a dens can occur as part of an atlas body of primitive, large size, then the dens should not be considered homologous with the atlas body. The identification of the small atlantal protuberance of cynodonts as a dens would certainly be questionable were there no other corroborative evidence. However, two independent lines of evidence support the contention that the cynodont atlantal protuberance is indeed a dens. The fkst of these concerns the evolution of mammalian apical ligament which unites the apex of the dens to the basioccipital bone. Developmentally, this ligament is derived from a notochordal remnant present at the atlanto-occipital level (Hecker, '23; Goodrich, '30: fig. 61; Gadow, '33). The developmental fate of this section of the embryonic notochord is therefore quite different from that between other vertebrae where it contributes to the nucleus pulposus (Williams, ' 0 8 ) . In terms of special relationships, the apical ligament is a notochordal remnant situated dorsal to other notochordal remnants represented by each nucleus pulposus. In primitive fossil reptiles, the notochordal remnant between the first cervical vertebral body and the occipital condyle was not situated dorsal to all other notochordal remnants. Instead, the position of the notochordal fossae on the cranial aspect of the first cervical body and on the caudal aspect of the occipital condyle is evidence that the notochordal remnant was in direct line with those following ( c f .Romer, ' 5 6 ) . Both the nucleus pulposus of mammals and the inferred notochordal remnant of certain primitive fossil and living reptiles occupy a centric position relative to the vertebral bodies, i.e., along a craniocaudal axis through the centers of the bodies. The mammalian apical ligament, however, represents a notochordal remnant that is eccentric in position, for in the adult mammal the apical ligament lies dorsal to a Abbreviations cl,cz, corpus or body of first and second cervical vertebrae d, dens or odontoid process fca, cranial articular facets of the axis icl, icz, intercentrum of first and second cervical vertebrae j, joint between bodies of first and second cervi- cal vertebrae nf, notochordal fossa oc, occipital condyle or condyles pa, proatlas ossicle Val, Val, vertebral arch of the first and second cervical vertebrae Fig. 1 Occipital condyle and atlas-axis evolution from pelycosaurs to mammals. Left hand column: occipital views of the skulls of A, a; pelycosaur, Dimetrodon; D, a cynodont, Cynognuthus; G, a monotreme, Omithorhynchus; L, a metatherian, Didelphis. Center column: left lateral views of atlas-axis components in B, a pelycosaur, Ophiacodon; E, a cynodont, Galesaurus; H, axis of a tritylodont, Oligokyphus; I, axis of Omithorhynchus; M, axis of Didelphis. Right hand column: anterior views of atlas body in C, Ophiucodon; F, Galesaurus; dorsal view of axis body in J, Okligokyphus; K, Omithorhynchus; N, Didelphis. Figures not to scale. A,B,C, after Romer and Price, '40; D, after Brofi and Schriider, '34; H, J, after Kuhne, '56. 177 THE MAMMALIAN DENS A C 8 nf oc 'C2 Pelycosaur stage D F E va Cynodont stage K oc y 'd Tritylodont- monotreme stage L M N d I oc M e t a therian-eutherian stage Figure 1 178 FARISH A. JENKINS, JR. craniocaudal axis through the vertebral bodies. The evolution of the apical ligament involves a dorsal displacement of the atlanto-occipital notochordal remnant relative to all other remnants (i.e., the nuclei puZposi) which retain their primitive, centric position. The dorsal displacement of the atlantooccipital notochord segment was already under way in pelycosaurs. The eccentric positions of the notochordal fossae of the occipital condyle and cranial aspect of the atlas body (fig. 1A,C) in pelycosaurs certainly attest to this displacement. Moreover, the reduced size of the atlanto-occipital notochordal fossae relative to postatlantal fossae is evidence that the associated notochordal remnant was at least smaller and perhaps altered in structure and function. In cynodonts, the loss of atlanto-occipital notochordal fossae r e p resents the culmination of the pelycosaurian trend toward the size reduction of these fossae. With the loss of the fossae, what became of the notochordal remnant? The well known developmental origin of the mammalian apical ligament is proof enough that the atlanto-occipital section of the embryonic notochord was never lost. In cynodonts, the dorsomedian protuberance on the cranial aspect of the atlantal body is situated in a position which might be expected of a notochordal fossa in an advanced pelycosaur. Thus, the protuberance may be reasonably interpreted to have been associated with the persistent atlantooccipital notochordal remnant. Likewise the atlanto-occipital notochordal remnant of the adult cynodont, no longer confined within the notochordal fossae, must have been different structurally and functionally from other notochordal remnants which retained their primitive relationship to amphicoelous vertebrae. The protuberance in cynodonts probably records the presence of a ligament. Whether ligamentous or not, the notochordal remnant in cynodonts became associated with a convexity rather than a concavity. In this sense the protuberance of cynodonts may represent an incipient dens. A second line of evidence supporting the above interpretation is derived from other fossil and recent forms representing structurally more advanced stages in the evolu- tion of the dens. A fossil form of particular interest is Oligokyphus, a tritylodont. The tritylodonts were a n advanced group of mammal-like reptiles, although they were not mammalian ancestors themselves. Kuhne ( ’ 5 6 ) has shown that Oligokyphus possessed an atlas centrum of large, primitive size (fig. lH,J); the bodies of the atlas and axis vertebrae were synostosed (fig. 1J). But in place of the slight protuberance of cynodonts is a dens of typically mammalian proportions, ie., a bony, peg-like projection (d, fig. lH,J). In all other respects the bodies of this tritylodont’s axis and atlas vertebrae are similar to those in cynodonts. The only significant difference is the extension of the cynodont protuberance into a “mammalian” dens. Since, on evidence of cranial osteology, the tritylodonts are thought to have been derived from cynodonts (Kuhne, ’ 5 6 ) , it is difficult to oppose the conclusion that the cynodont protuberance is the precursor of the dens. The fossil record of the earliest (it-., Triassic) mammals is represented mostly by teeth and jaws; to date, no atlas-axis components have been recovered. It is probable, however, that the morphology of the dens of earliest mammals was similar to that in Mtylodonts. The evidence for such a conclusion is based on the morphological similarity between the tritylodont axis and the axis characteristic of the most primitive mammals surviving today, the monotremes. The order Monotremata includes both the platypus (Omithorhynchus anatinus) and the spiny anteaters or echidnas (various species of the genera Tachyglossus and Zagbssus). In the platypus, for example, the dens is of typical mammalian size and proportions (d, fig. 11). But between the dens and the axis body (cz, fig. 11) is a bulbous ossification (cl, fig. 11) which bears the articular facets for the atlas. In position, shape and relations, this ossification is extremely similar to both the cynodont and the tritylodont atlas centrum. Moreover, it is joined to the axis body along a distinct joint (j, fig. 11,K) as in cynodonts and tritylodonts. The conclusion is unavoidable that this ossification is the atlas body, and that the dens is merely a process aris- 179 THE MAMMALIAN DENS ing from it. Therefore, the two cannot be homologous. The joint between the synostosed atlantal and axial bodies of pre-mammals and monotremes delineates the boundaries of originally separate but articulating ossifications. If the dens of advanced mammals, i.e., marsupials and eutherians, represents the only vestige of the atlas centrum in these groups (as is generally claimed), then a joint might be expected to occur at the base of the dens. Such a joint would represent the plane of synostosis of the first two cervical vertebral bodies. In fact, however, a joint is never found transecting the base of the dens. In representative genera of all living families of marsupials, a joint transversely divides the ‘‘body” of the axis in a plane posterior to the cranial articular facets. In a few genera, the joint transects the dorsolateral corners of the facets (j, fig. 1M,N) but elsewhere lies entirely posterior to them. The position of the joint posterior to the cranial articular facets of the axis signifies that the atlas ring retains its original primitive articular relationship. In pelycosaurs and cynodonts, the separate atlas arches and intercentrum articulated with the atlas body. Among modern mammals, the atlas arches and intercentrum synostose to form a bony ring which is the atlas; yet in monotremes and marsupials, the atlas ring still articulates with the primitive atlas body, i.e., on facets lying anterior to the transverse joint of the axis. The axes of eutherian mammals are morphologically rather variable between orders and even between families. Yet even in the most specialized forms, the transverse joint of the axis does not occur across the base of the dens. There is invariably a sizable osseous body caudal to the dens and cranial to the transverse joint which represents the atlas body- although much diminished in size and completely altered in form from that in cynodonts and monotremes (cl, fig. 2). The tendency to reduce the atlas body is accompanied by a displacement of part of cranial articular facets onto the actual body of the axis. Thus, in some eutherians, the transverse joint bisects the cranial facets (fig. 2B). In other groups, the greater part of the facets are borne by the axis (fig. 2C). But even in the most highly modified forms, such as man (fig. 2F), the dens alone is not the sole vestige of the atlas body. Even in those mammals in which the cranial articular facets are formed entirely from axis elements, a post-dens ossification - the vestige of the original atlas body is retained. The development of the dens in the opossum, Didelphis marsupialis, may now be evaluated in light of the paleontological and comparative morphological evidence which supports the conclusion that the dens arises as an extension of the primitive atlas body. The earliest section available is from a pouch young 20 days post partum (fig. 3). At this stage the completely cartilaginous dens is characterized by two zones of hypertrophied chondrocytes. The dens is recognizable as a bulbous excrescence on the anterior of the two zones. From the apex of the developing dens runs a connective tissue strand which later forms the apical ligament. There is no indication at this stage that the dens develops as a structure independent of the cartilaginous anlage of the atlas body. The second stage is from a pouch young of about 25 days post partum (fig. 4). The ossifying axis body is clearly set off from that of C3 and from an anterior ossification (representing the atlas body) by the developing intervertebral discs. The dens is still cartilaginous, and is developing in conjunction with a large center of ossification interpreted as serially homologous with the other ossifying bodies. Parasagittal sections show that the dens is the apex of a broad-based, triangular mass of cells, of which the ossification center noted above forms the largest part. The third and fourth stages are represented by skeletal preparations of pouch young estimated to be 50 and 70 days post partum. In the 50 day old specimen (fig. 5A), the axis consists of four unfused ossifications: the two vertebral arch halves, the axis body, and the atlas body with the dens. The atlas body is a triangular ossicle, the blunt apex of which is directly anteriorly. The differentiation of the dens as a peg-like, bony structure has just begun. In the 70 day old specimen (fig. - 180 FARISH A. JENKINS, JR. C. 8. A. ca fca f ca d E. 0. F: a fca I d Fig. 2 Dorsal view of the axis in various juvenile mammals to show the position of the transverse joint ( j ) . A an echidna (Tachyglossus aculeatus), YPMOC 1961. B, dog (Canis familiaris), six months old, YPMOC 2600. C, pig (Sus s c f o f a ) ,YPMOC 1580. D, an armadillo, (Dasyps nouemcinctus), YPMOC 2333. E, 12 day old colt (Equus caballus), YPMOC 198. F, man (Homo sapiens), AMNH 99-8594, approximately seven years old. Not to scale. Abbreviations as in figure 1. SB), the vertebral arches have nearly completed synostosis. The axis is not yet synostosed to the vertebral arches nor to the atlas body ossicle. The dens appears as a process arising from the atlas body ossicle of which it is small part. The fifth and last stage is represented by an osteological preparation of a young adult opossum estimated to be six months old (fig. 5C). In this specimen the dens is but a small process arising from the atlas body. The atlas body ossification, as in other marsupials, forms the anterior third of the axis body, and includes the cranial articular facets. The joint between the atlas body ossification and the axis body is clearly visible. The developmental history of the opossum dens demonstrates that the dens alone cannot be considered the homologue of the primitive atlas body, as is so often implied or stated. It is indisputable that the dens originates in conjunction with an embryonic structure, the so-called atlas body ossicle, which is homologous in position with the atlas body anlage of primitive tetrapods. The dens as a distinct process is most appropriately regarded as neomorphic. DISCUSSION Only a few authors have recognized the relevance of the transverse joint of the axis in delineating the axial and atlantal bodies. W. H. Flower (1885) reported that .if the axis [of a mammal] is examined a year or two after birth, its body appears to be composed of two parts, one placed in front of the other, the fmt including the odontoid process [dens] and the anterior part of the body, the second all the remainder of the body." Flower drew no fur- ". . THE MAMMALIAN D E N S 181 Fig. 3 Sagittal section through the atlas and axis bodies of opossum (Didelphis marsupialis) pouch young 20 days post partum (Wistar Institute Ser. cat. No. 17683). x 35. The two adjacent zones of hypertrophied chondrocytes represent the axis body (C2) and the atlas body ((21). The developing dens is indicated ( d ) . Below and to the right of the dens is a section through the atlas intercentrum which will form the ventral part of the atlas ring. Fig. 4 Sagittal section through the atlas and axis bodies of opossum (Didelphis marsupialis) pouch young 25 days post partum. x 40. The two adjacent zones of ossification represent the axis body ( C , ) and the atlas body (C,). The cartilaginous extension to the right from the atlas body represents the developing dens ( d ) . Below the dens is a section through the atlantal intercentrum which will form the ventral part of the atlas ring. 182 FARISH A. JENKINS, JR. A c: 6, B C Fig. 5 The development of ossification in the axis of the opossum, Didelphis marsupialis, to demonstrate that the dens ( d ) arises in conjunction with the ossicle representing the primitive atlas body (cI). Left column, lateral views; right column, dorsal views. A, pouch young opossum, YPMOC 5502, estimated to be 50 days post parturn; approximately x 3.25. B, pouch young opossum, YPMOC 5331, estimated to be 70 days post partum; approximately X 3.25. C, young adult opossum, YPMOC 243; approximately x 1.2. ther conclusions from this observation, except to propose that the posterior extremity of the odontoid ossification represents the “usual disk-like epiphyses of the vertebral bodies.” Gadow (’33) objected to these observations on the ground that Flower “. . .looked upon the odontoid as part of the axis centrum instead of a centrum in its own right.. .”. In fact, Flower did not reject the homology of the odontoid and atlas body, but implied, although somewhat indirectly, that more than just the odontoid process was homologous to the atlas body. Subsequently, Rueger ( ’ 3 8 ) examined the axial joint patterns in a variety of mammals. He observed that in all cases at least part if not all of the cranial articular facets of the axis arose from the atlas body. But even with this evidence in hand, he did not challenge the concept of the atlas bodydens homology. More recently, Brocher (’55) repeated Rueger’s observation that “. . .Strenggenommen bildet der urspriingliche Wirbelkorper des Atlas nicht nur den spateren Processus odontoideus, sondern auch einen Teil des Epistropheuskorpers.” The failure to exploit this evidence fully, and to reveal the actual relationship of the dens and atlas body, may be attributed to a dependence on developmental evidence alone. The function of the dens will now be briefly discussed with reference to its evolutionary origin. Rockwell et al. (’38) and Slijper (’46) have shown that the mechanics of cervical vertebrae are analogous to a loaded beam supported at one end only. In quadrupedal animals, the bodies may be regarded as compression-resisting members, and the vertebral arches, their processes and associated ligaments as tensionresisting members. In the evolutionary lineage leading to mammals, the first two cervical vertebrae became specialized to permit an increased amount of cranial mobility. Movement at the atlanto-axial joint is virtually restricted to rotation of the atlas (and cranium) on the axis. In order to achieve atlanto-axial rotation, the articular processes joining the atlas and axis must be lost altogether because their contact would only serve to prevent rotation. However, loss of the atlanto-axial articular processes also entails loss of a principal tension-resisting mechanism at this joint. The weight of the head, which tends to flex the cervical series, would be the factor inducing a disproportionate amount of stress at the atlanto-axial joint relative to other cervical joints. The dens and its associated ligaments in effect substitute for the lost atlanto-axial articular processes. These structures do not inhibit rotation because they reinforce the joint along its axis of rotation. This arrangement prevents the atlas (and head) from flexing on the axis, or, in other words, acts as a tension-resisting mechanism (and is probably less flexible than that of other cervical articular joints). THE MAMMALIAN DENS In pelycosaurs the presence of well developed atlanto-axial articular processes prohibited rotation at the atlanto-axial joint. In cynodonts, however, the cranial articular processes of the axis are vestigial and the caudal process of the atlas are altogether lost. Atlanto-axial rotation was clearly possible. The vestigial cranial articular processes on the axis probably represent the attachment of some ligamentous or other connective tissue strand which only incompletely sustained the tensional forces generated by the weight of the head. The remainder of the tensional forces were undoubtedly accommodated by the incipient dens and its associated ligaments. Many authors state that the dens acts as an “axis” or pivot about which the atlas rotates. While this analogy is convenient in describing the movement involved, it carries a misleading functional connotation. The atlas can and does rotate on the axis in cases where the dens is congenitally absent or separate from the axis. In reported cases of congenital absence of the dens in man (cf. Fullenlove, ’54, and other authors cited by him), the anomaly gave no symptoms until, through accident or during the course of normal exercise, more than usual stress was brought to bear on the head and neck. Subluxation of the atlas, sometimes accompanied by neurological symptoms, was the common result. Werne (‘57) reported similar cases in which “insufficiency” of the transverse ligament also permitted atlas dislocation. The normal function of such an atlanto-axial joint in the absence of injury may be attributed to the fact that the function of the dens and transverse ligament is to reinforce against flexing stresses. The vertical posture and shortness of the human neck tends to minimize these stresses, and therefore the dens defect is manifest only when such stresses are increased. In quadrupedal mammals, and especially in those that employ powerful movements of head and neck in feeding and other activities, the selective disadvantages of a congenitally absent or separated dens must be great. ACKNOWLEDGMENTS I have been greatly aided by advice and constructive criticism from Dr. E. S . Crelin of the Department of Anatomy, Yale Uni- 183 versity School of Medicine, and by technical assistance from Mr. E. V. Newton. Professor A. W. Crompton of Yale University generously provided facilities for the completion of this study, and provided helpful guidance in my study of cynodont therapsids. I am grateful to Dr. F. R. Parrington, F.R.S., for the loan of fossil specimens from the University Museum of Zoology, Cambridge, and to Dr. A. J. 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