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UNIVERSITY OF KANSAS PUBLICATIONS

MUSEUM OF NATURAL HISTORY


Volume 12, No. 15, pp. 657-680, 11 figs.
May 18, 1964


The Adductor Muscles of the Jaw
In Some Primitive Reptiles


BY

RICHARD C. FOX


UNIVERSITY OF KANSAS
LAWRENCE
1964


UNIVERSITY OF KANSAS PUBLICATIONS, MUSEUM OF NATURAL HISTORY

Editors: E. Raymond Hall, Chairman, Henry S. Fitch,
Theodore H. Eaton, Jr.


Volume 12, No. 15, pp. 657-680, 11 figs.
Published May 18, 1964


UNIVERSITY OF KANSAS
Lawrence, Kansas


PRINTED BY
HARRY (BUD) TIMBERLAKE, STATE PRINTER
TOPEKA, KANSAS
1964

30-1522




The Adductor Muscles of the Jaw
In Some Primitive Reptiles

BY

RICHARD C. FOX


Information about osteological changes in the groups of reptiles that
gave rise to mammals is preserved in the fossil record, but the
musculature of these reptiles has been lost forever. Nevertheless, a
reasonably accurate picture of the morphology and the spatial
relationships of the muscles of many of these extinct vertebrates can
be inferred by studying the scars or other marks delimiting the origins
and insertions of muscles on the skeletons of the fossils and by
studying the anatomy of Recent genera. A reconstruction built by these
methods is largely speculative, especially when the fossil groups are
far removed in time, kinship and morphology from Recent kinds, and when
distortion, crushing, fragmentation and overzealous preparation have
damaged the surfaces associated with the attachment of muscles. The
frequent inadequacy of such direct evidence can be partially offset by
considering the mechanical demands that groups of muscles must meet to
perform a particular movement of a skeletal member.

Both direct anatomical evidence and inferred functional relations were
used to satisfy the purposes of the study here reported on. The
following account reports the results of my efforts to: 1, reconstruct
the adductor muscles of the mandible in _Captorhinus_ and _Dimetrodon_;
2, reconstruct the external adductors of the mandible in the cynodont
_Thrinaxodon_; and 3, learn the causes of the appearance and continued
expansion of the temporal fenestrae among the reptilian ancestors of
mammals.

The osteology of these three genera is comparatively well-known.
Although each of the genera is somewhat specialized, none seems to have
departed radically from its relatives that comprised the line leading
to mammals.

I thank Prof. Theodore H. Eaton, Jr., for suggesting the study here
reported on, for his perceptive criticisms regarding it, and for his
continued patience throughout my investigation. Financial assistance
was furnished by his National Science Foundation Grant (NSF-G8624) for
which I am also appreciative. I thank Dr. Rainer Zangerl, Chief Curator
of Geology, Chicago Museum of Natural History, for permission to
examine the specimens of _Captorhinus_ and _Dimetrodon_ in that
institution. I am grateful to Mr. Robert F. Clarke, Assistant Professor
of Biology, The Kansas State Teachers College, Emporia, Kansas, for the
opportunity to study his specimens of _Captorhinus_ from Richard's
Spur, Oklahoma. Special acknowledgment is due Mr. Merton C. Bowman for
his able preparation of the illustrations.


Captorhinus

The outlines of the skulls of _Captorhinus_ differ considerably from
those of the skulls of the primitive captorhinomorph _Protorothyris_.
Watson (1954:335, Fig. 9) has shown that in the morphological sequence,
_Protorothyris--Romeria--Captorhinus_, there has been flattening and
rounding of the skull-roof and loss of the primitive "square-cut"
appearance in transverse section. The quadrates in _Captorhinus_ are
farther from the midline than in _Protorothyris_, and the adductor
chambers in _Captorhinus_ are considerably wider than they were
primitively. Additionally, the postorbital region of _Captorhinus_ is
relatively longer than that of _Protorothyris_, a specialization that
has increased the length of the chambers within.

In contrast with these dimensional changes there has been little shift
in the pattern of the dermal bones that roof the adductor chambers. The
most conspicuous modification in _Captorhinus_ is the absence of the
tabular. This element in _Protorothyris_ was limited to the occiput and
rested without sutural attachment upon the squamosal (Watson,
1954:338); later loss of the tabular could have had no effect upon the
origins of muscles from inside the skull roof. Changes in pattern that
may have modified the origin of the adductors in _Captorhinus_ were
correlated with the increase in length of the parietals and the
reduction of the supratemporals. Other changes that were related to the
departure from the primitive romeriid condition of the adductors
included the development of a coronoid process, the flattening of the
quadrate-articular joint, and the development of the peculiar dentition
of _Captorhinus_.

The adductor chambers of _Captorhinus_ are large. They are covered
dorsally and laterally by the parietal, squamosal, postfrontal,
postorbital, quadratojugal and jugal bones. The chamber extends
medially to the braincase, but is not limited anteriorly by a bony
wall. The occiput provides the posterior limit. The greater part of the
adductor chambers lies mediad of the mandibles and thus of the
Meckelian fossae; consequently the muscles that arise from the dermal
roof pass downward and outward to their insertion on the mandibular
rami.


_Mandible_

The mandibular rami of _Captorhinus_ are strongly constructed. Each
ramus is slightly convex in lateral outline. Approximately the anterior
half of each ramus lies beneath the tooth-row. This half is roughly
wedge-shaped in its lateral aspect, reaching its greatest height
beneath the short posterior teeth.

The posterior half of each ramus is not directly involved in supporting
the teeth, but is associated with the adductor musculature and the
articulation of the ramus with the quadrate. The ventral margin of this
part of the ramus curves dorsally in a gentle arc that terminates
posteriorly at the base of the retroarticular process. The dorsal
margin in contrast sweeps sharply upward behind the teeth and continues
posteriorly in a long, low, truncated coronoid process.

A prominent coronoid process is not found among the more primitive
members of the suborder, such as _Limnoscelis_, although the mandible
commonly curves upward behind the tooth-row in that genus. This area in
_Limnoscelis_ is overlapped by the cheek when the jaw is fully adducted
(Romer, 1956:494, Fig. 213), thereby foreshadowing the more extreme
condition in _Captorhinus_.

The coronoid process in _Captorhinus_ is not oriented vertically, but
slopes inward toward the midline at approximately 45 degrees,
effectively roofing the Meckelian fossa and limiting its opening to the
median surface of each ramus. When the jaw was adducted, the coronoid
process moved upward and inside the cheek. A space persisted between
the process and the cheek because the process sloped obliquely away
from the cheek and toward the midline of the skull. The external
surface of the process presented an area of attachment for muscles
arising from the apposing internal surface of the cheek.


_Palate_

The palate of _Captorhinus_ is of the generalized rhynchocephalian type
(Romer, 1956:71). In _Captorhinus_ the pterygoids and palatines are
markedly arched and the relatively large pterygoid flange lies almost
entirely below the lower border of the cheek. The lateral edge of the
flange passes obliquely across the anterior lip of the Meckelian fossa
and abuts against the bottom lip of the fossa when the jaw is closed.

The palatines articulate laterally with the maxillary bones by means of
a groove that fits over a maxillary ridge. This presumably allowed the
halves of the palate to move up and down rather freely. The greatest
amplitude of movement was at the midline. Anteroposterior sliding of
the palate seems impossible in view of the firm palatoquadrate and
quadrate-quadratojugal articulations.

The subtemporal fossa is essentially triangular, and its broad end is
bounded anteriorly by the pterygoid flange. The fossa is lateral to
much of the adductor chamber; consequently muscles arising from the
parietals passed ventrolaterally, parallel to the oblique quadrate
ramus of the pterygoid, to their attachment on the mandible.


_Musculature_

These osteological features indicate that the adductor muscles of the
jaw in _Captorhinus_ consisted of two primary masses (Figs. 1, 2, 3).
The first of these, the capitimandibularis, arose from the internal
surface of the cheek and roof of the skull and inserted on the bones of
the lower jaw that form the Meckelian canal and the coronoid process.

[Illustration: FIG. 1. _Captorhinus._ Internal aspect of skull, showing
masseter, medial adductor, and temporal muscles. Unnumbered specimen,
coll. of Robert F. Clarke. Richard's Spur, Oklahoma. × 2.]

[Illustration: FIG. 2. _Captorhinus._ Internal aspect of skull, showing
anterior and posterior pterygoid muscles. Same specimen shown in Fig.
1. × 2.]

The muscle was probably divided into a major medial mass, the temporal,
and a lesser, sheetlike lateral mass, the masseter. The temporal was
the largest of the adductors and arose from the lateral parts of the
parietal, the dorsal parts of the postorbital, the most posterior
extent of the postfrontal, and the upper parts of the squamosal. The
muscle may have been further subdivided, but evidence for subordinate
slips is lacking. The fibers of this mass were nearly vertically
oriented in lateral aspect since the parts of the ramus that are
available for their insertion lie within the anteroposterior extent of
the adductor chamber. In anterior aspect the fibers were obliquely
oriented, since the jaw and subtemporal fossa are lateral to much of
the skull-roof from which the fibers arose.

The masseter probably arose from the quadratojugal, the jugal, and
ventral parts of the squamosal, although scars on the quadratojugal and
jugal are lacking. The squamosal bears an indistinct, gently curved
ridge, passing upward and forward from the posteroventral corner of the
bone and paralleling the articulation of the squamosal with the
parietal. This ridge presumably marks the upper limits of the origin of
the masseter from the squamosal.

[Illustration: FIG. 3. _Captorhinus._ Cross-section of right half of
skull immediately behind the pterygoid flange, showing masseter,
temporal, and anterior pterygoid muscles. Same specimen shown in Fig.
1. × 2.]

[Illustration: FIG. 4. _Captorhinus._ Internal aspect of left
mandibular fragment, showing insertion of posterior pterygoid muscle.
KU 8963, Richard's Spur, Oklahoma. × 2.8.]

The masseter inserted on the external surface of the coronoid process,
within two shallow concavities separated by an oblique ridge. The
concavities and ridge may indicate that the muscle was divided into two
sheets. If so, the anterior component was wedge-shaped in
cross-section, and its thin posterior edge overlapped the larger mass
that inserted on the posterior half of the coronoid process.

From a functional standpoint it is doubtful that a major component of
the adductors arose from the quadrate wing of the pterygoid, for when
the jaw is closed the Meckelian fossa is directly lateral to that bone.
If the jaw were at almost any angle but maximum depression, the
greatest component of force would be mediad, pulling the rami together
and not upward. The mediad component would increase as the jaw
approached full adduction. Neither is there anatomical evidence for an
adductor arising from the quadrate wing of the pterygoid. The bone is
smooth, hard, and without any marks that might be interpreted as muscle
scars.

The internal adductor or pterygoid musculature in _Captorhinus_
consisted of anterior and posterior components. The anterior pterygoid
arose from the lateral edge and the dorsal surface of the pterygoid
flange. The burred dorsal recurvature of the edge resembles that of the
flange of crocodiles, which serves as part of the origin of the
anterior pterygoid in those animals. In _Captorhinus_ the attachment of
the anterior pterygoid to the edge of the flange was probably
tendinous, judging from the extent of the development of the edge of
the flange. From the edge the origin extended medially across the
dorsal surface of the flange; the ridging of this surface is
indistinct, leading to the supposition that here the origin was more
likely to have been fleshy than tendinous.

The anterior pterygoid extended obliquely backward and downward from
its origin, passed medial to the temporal muscle and inserted on the
ventral and medial surfaces of the splenial and angular bones beneath
the Meckelian fossa. The spatial relationship between the palate and
quadrate-articular joint indicate that the muscle was probably a minor
adductor in _Captorhinus_.

When the jaw was adducted, the insertion of the anterior pterygoid was
in a plane nearly level with the origin. Contraction of the anterior
pterygoid when the jaw was in this position pulled the mandible forward
and did not adduct it. Maximum depression of the mandible produced
maximum disparity vertically between the levels of the origin and
insertion. The force exerted by the anterior pterygoid upon the
mandible when fully lowered most nearly approached the perpendicular to
the long axes of the mandibular rami, and the resultant force acting on
the mandible was adductive.

The adductive component of force therefore decreased as the jaw swung
upward, with the result that the anterior pterygoid could only have
been active in initiating adduction and not in sustaining it.

The evidence regarding the position and extent of the posterior
pterygoid is more veiled. On the medial surface of the mandible, the
prearticular and articular bones meet in a ridge that ventrally rims
the glenoid cavity (Fig. 4). The ridge extends anteriorly and curves
slightly in a dorsal direction and meets the Meckelian fossa. The
curved part of the ridge is made of the prearticular bone alone. A
small hollow above the ridge, anterior to the glenoid cavity, faces the
medial plane of the skull and is bordered by the articular bone behind
and above, and by the Meckelian fossa in front.

The surfaces of the hollow and the prearticular-articular ridge bear
tiny grooves and ridges that seem to be muscle scars. The entire area
of the hollow and its bordering features was probably the area of
insertion of the posterior pterygoid.

However, the area of insertion lies mostly ventral to the articulating
surface of the articular bone and extends but slightly in front of it.
Seemingly little lever effect could be exercised by an adductor
attaching in this position, namely, at the level of the fulcrum of the
mandibular ramus.

The posterior pterygoid muscle probably arose from the anterior portion
of the pterygoid wing of the quadrate, from a ridge on the ventromedial
surface. From the relationship of the muscle to the articulation of the
jaw with the skull, it may be deduced that the muscle was limited in
function to the stabilization of the quadrate-articular joint by
keeping the articular surfaces in close contact with each other and by
preventing lateral slipping.

Finally there is evidence for an adductor between the temporal and
masseter masses. The anterior dorsal lip of the Meckelian fossa
supports a small knob to which this muscle attached, much as in
_Sphenodon_ (Romer, 1956:18, Fig. 12). Presumably the muscle was
sheetlike and attached to the skull roof, medial to the attachment of
the masseter.

A pseudotemporal may have been present, but evidence to indicate its
extent and position is lacking. The muscle usually arises from the
epipterygoid and nearby areas of the braincase and skull roof and
inserts in the anterior parts of the fossa of the jaw. In _Captorhinus_
the lateral wing of the pterygoid cuts across the fossa, effectively
blocking it from the upper and medial parts of the skull, the areas of
origin for the pseudotemporal.


Dimetrodon

The morphology of the skull of _Dimetrodon_ closely resembles that of
the primitive _Haptodus_ (Haptodontinae, Sphenacodontidae), and "hence
may be rather confidently described as that of the family as a whole"
(Romer and Price, 1940:285). The major differences between the two
genera are in the increased specialization of the dentition, the
shortening of the lacrimal, and the development of long vertebral
spines in _Dimetrodon_. The absence of gross differences in the areas
of the skull associated with the groups of muscles with which this
study is concerned, implies a similarity in the patterns of musculature
between the two groups. Romer and Price suggest that _Haptodus_,
although too late in time to be an actual ancestor, shows "all the
common features of the _Dimetrodon_ group on the one hand and the
therapsids on the other." The adductors of the jaw of _Dimetrodon_ were
probably little changed from those of the Haptodontinae and represent a
primitive condition within the suborder.

_Dimetrodon_ and _Captorhinus_ differ in the bones associated with the
adductor mechanism; the area behind the orbit in _Dimetrodon_ is
relatively shorter, reducing the comparative longitudinal extent of the
adductor chamber. Furthermore, the dermal roof above the adductor
chamber slopes gently downward from behind the orbit to its contact
with the occipital plate in _Dimetrodon_. Temporal fenestrae are, of
course, present in _Dimetrodon_.


_Musculature_

The adductor musculature of the lower jaw in _Dimetrodon_ was divided
into lateral and medial groups (Figs. 5, 6). The lateral division
consisted of temporal and masseter masses. The temporal arose from the
upper rim of the temporal opening, from the lateral wall of the skull
behind the postorbital strut, and from the dorsal roof of the skull.
The bones of origin included jugal, postorbital, postfrontal, parietal
and squamosal. This division may also have arisen from the fascia
covering the temporal opening (Romer and Price, 1940:53). The muscle
passed into the Meckelian fossa of the mandible and inserted on the
angular, surangular, prearticular, coronoid and dentary bones.
Insertion on the lips of the fossa also probably occurred.

The lateral division arose from the lower rim of the temporal opening
and from the bones beneath. Insertion was in the Meckelian fossa and
on the dorsal surface of the adjoining coronoid process.

[Illustration: FIG. 5. _Dimetrodon._ Internal aspect of skull, showing
masseter and temporal muscles. Skull modified from Romer and Price
(1940). Approx. × 1/4.]

The reconstruction of the progressively widening masseter as it
traveled to the mandible follows from the progressively widening
depression on the internal wall of the cheek against which the muscle
must have been appressed. The depressed surface included the posterior
wing of the jugal, the whole of the squamosal, and probably the
anteriormost parts of the quadratojugal. Expansion of the muscle
rostrally was prevented by the postorbital strut that protected the
orbit (Romer and Price, 1940:53).

The sphenacodonts possess the primitive rhynchocephalian kind of
palate. In _Sphenodon_ the anterior pterygoid muscle arises from the
dorsal surface of the pterygoid bone and from the adjacent bones. A
similar origin suggests itself for the corresponding muscle, the second
major adductor mass, in _Dimetrodon_.

From the origin the muscle passed posterodorsad and laterad of the
pterygoid flange. Insertion was in the notch formed by the reflected
lamina of the angular, as suggested by Watson (1948).

In _Dimetrodon_ the relationship of the dorsal surface of the palate
and the ventromedial surface of the mandible in front of the
articulation with the quadrate is unlike that in _Captorhinus_. When
the mandible of _Dimetrodon_ is at rest (adducted), a line drawn
between these two areas is oblique, between 30 and 40 degrees from the
horizontal. Depression of the mandible increases this angle. The
insertion of the anterior pterygoid is thus always considerably below
the origin, permitting the muscle to be active throughout the movement
of the mandible, from maximum depression to complete adduction. This
was a major factor in adding substantially to the speed and power of
the bite.

The presence and extent of a posterior pterygoid is more difficult to
assess, because of the closeness of the glenoid cavity and the raised
ridge of the prearticular, and the occupancy of at least part of this
region by the anterior pterygoid. In some specimens of _Dimetrodon_ the
internal process of the articular is double (see Romer and Price,
1940:87, Fig. 16) indicating that there was a double insertion here.
Whether the double insertion implies the insertion of two separate
muscles is, of course, the problem. Division of the pterygoid into
anterior and posterior portions is the reptilian pattern (Adams, 1919),
and such is adhered to here, with the posterior pterygoid arising as a
thin sheet from the quadrate wing of the pterygoid and the quadrate,
and inserting by means of a tendon on the internal process of the
articular, next to the insertion of the anterior pterygoid.

[Illustration: FIG. 6. _Dimetrodon._ Internal aspect of right cheek,
showing anterior and posterior pterygoid muscles. Skull modified from
Romer and Price (1940). Approx. × 1/4.]

Watson (1948) has reconstructed the musculature of the jaw in
_Dimetrodon_ with results that are at variance with those of the
present study. Watson recognized two divisions, an inner temporal and
an outer masseteric, of the capitimandibularis, but has pictured them
(830: Fig. 4; 831: Fig. 5C) as both arising from the inner surface of
the skull roof above the temporal opening. But in _Captorhinus_ the
masseter arose from the lower part of the cheek close to the outer
surface of the coronoid process. Watson has shown (1948:860, Fig. 17B)
the same relationship of muscle to zygoma in _Kannemeyeria sp._ It is
this arrangement that is also characteristic of mammals and presumably
of _Thrinaxodon_. In view of the consistency of this pattern, I have
reconstructed the masseter as arising from the lower wall of the cheek
beneath the temporal opening.

Watson's reconstruction shows both the temporal and masseter muscles as
being limited anteroposteriorly to an extent only slightly greater than
the anteroposterior diameter of the temporal opening. The whole of the
posterior half of the adductor chamber is unoccupied. More probably
this area was filled by muscles. The impress on the inner surface of
the cheek is evident, and the extent of both the coronoid process and
Meckelian opening beneath the rear part of the chamber indicate that
muscles passed through this area.

Watson remarked (1948:829-830) that the Meckelian opening in
_Dimetrodon_ "is very narrow and the jaw cavity is very small. None the
less, it may have been occupied by the muscle or a ligament connected
to it. Such an insertion leaves unexplained the great dorsal production
of the dentary, surangular and coronoid. This may merely be a device to
provide great dorsal-ventral stiffness to the long jaw, but it is
possible and probable that some part of the temporal muscle was
inserted on the inner surface of the coronoid. Indeed a very
well-preserved jaw of _D. limbatus?_ (R. 105: Pl. I, Fig. 2) bears a
special depressed area on the outer surface of the extreme hinder end
of the dentary which differs in surface modelling from the rest of the
surface of the jaw, has a definite limit anteriorly, and may represent
a muscle insertion. The nature of these insertions suggests that the
muscle was already divided into two parts, an outer masseter and an
inner temporalis." But, unaccountably, Watson's illustration (1948:830,
Fig. 4) of his reconstruction limits the insertion of the temporal to
the anterior limit of the Meckelian opening and a part of the coronoid
process above it. No muscle is shown entering the Meckelian canal. It
seems more likely that the temporal entered and inserted in the canal
and on its dorsal lips. The masseter inserted lateral to it, over the
peak of the coronoid process, and overlapping onto the dorsalmost
portions of its external face, as Watson has illustrated (Plate I,
middle fig.).

I am in agreement with Watson's reconstruction of the origins for both
the anterior and posterior pterygoid muscles. On a functional basis,
however, I would modify slightly Watson's placement of the insertions
of these muscles. Watson believed that the jaw of _Dimetrodon_ was
capable of anteroposterior sliding. The articular surfaces of the jaws
of _Dimetrodon_ that I have examined indicate that this capability, if
present at all, was surely of a very limited degree, and in no way
comparable to that of _Captorhinus_. The dentition of _Dimetrodon_
further substantiates the movement of the jaw in a simple up and down
direction. The teeth of _Dimetrodon_ are clearly stabbing devices; they
are not modified at all for grinding and the correlative freedom of
movement of the jaw that that function requires in an animal such as
_Edaphosaurus_. Nor are they modified to parallel the teeth of
_Captorhinus_. The latter's diet is less certain, but presumably it was
insectivorous (Romer, 1928). With the requisite difference in levels of
origin and insertion of the anterior pterygoid in _Dimetrodon_ insuring
the application of force throughout the adduction of the jaws, it would
seem that the whole of the insertion should be shifted downward and
outward in the notch. If this change were made in the reconstruction,
the anterior pterygoid would have to be thought of as having arisen by
a tendon from the ridge that Watson has pictured (1948:828, Fig. 3) as
separating his origins for anterior and posterior pterygoids. The
posterior pterygoid, in turn, arose by tendons from the adjoining
lateral ridge and from the pterygoid process of Romer and Price.
Tendinous origins are indicated by the limitations of space in this
area, by the strength of the ridges pictured and reported by Watson,
and by the massiveness of the pterygoid process of Romer and Price.


Discussion

A comparison of the general pattern of the adductor musculature of
_Captorhinus_ and _Dimetrodon_ reveals an expected similarity. The
evidence indicates that the lateral and medial temporal masses were
present in both genera. The anterior pterygoid aided in initiating
adduction in _Captorhinus_, whereas in _Dimetrodon_ this muscle was
adductive throughout the swing of the jaw. Evidence for the presence
and extent of a pseudotemporal muscle in both _Captorhinus_ and
_Dimetrodon_ is lacking. The posterior division of the pterygoid is
small in _Captorhinus_. In _Dimetrodon_ this muscle has been
reconstructed by Watson as a major adductor, an arrangement that is
adhered to here with but slight modification.

The dentition of _Captorhinus_ suggests that the jaw movement in
feeding was more complex than the simple depression and adduction that
was probably characteristic of _Dimetrodon_ and supports the
osteological evidence for a relatively complex adductor mechanism.

In _Captorhinus_ the presence of an overlapping premaxillary beak
bearing teeth that are slanted posteriorly requires that the mandible
be drawn back in order to be depressed. Conversely, during closure, the
jaw must be pulled forward to complete full adduction. The
quadrate-articular joint is flat enough to permit such anteroposterior
sliding movements. The relationship of the origin and insertion of the
anterior pterygoid indicates that this muscle, ineffective in
maintaining adduction, may well have acted to pull the mandible
forward, in back of the premaxillary beak, in the last stages of
adduction. Abrasion of the sides of the inner maxillary and outer
dentary teeth indicates that tooth-to-tooth contact did occur. Whether
such abrasion was due to contact in simple vertical adduction or in
anteroposterior sliding is impossible to determine, but the evidence
considered above indicates the latter probability.

Similarities of _Protorothyris_ to sphenacodont pelycosaurs in the
shape of the skull and palate already commented upon by Watson (1954)
and Hotton (1961) suggest that the condition of the adductors in
_Dimetrodon_ is a retention of the primitive reptilian pattern, with
modifications mainly limited to an increase in size of the temporalis.
_Captorhinus_, however, seems to have departed rather radically from
the primitive pattern, developing specializations of the adductors that
are correlated with the flattening of the skull, the peculiar marginal
and anterior dentition, the modifications of the quadrate-articular
joint, and the development of the coronoid process.


Thrinaxodon

The evidence for the position and extent of the external adductors of
the lower jaw in _Thrinaxodon_ was secured in part from dissections of
_Didelphis marsupialis_, the Virginia opossum. Moreover, comparison of
the two genera reveals striking similarities in the shape and spatial
relationships of the external adductors. These are compared below in
some detail.

The sagittal crest in _Thrinaxodon_ is present but low. It arises
immediately in front of the pineal foramen from the confluence of
bilateral ridges that extend posteriorly and medially from the base of
the postorbital bars. The crest diverges around the foramen, reunites
immediately behind it, and continues posteriorly to its junction with
the supraoccipital crest (Estes, 1961).

In _Didelphis_ the sagittal crest is high and dorsally convex in
lateral aspect, arising posterior to and medial to the orbits, reaching
its greatest height near the midpoint, and sloping down to its
termination at the supraoccipital crest. Two low ridges extend
posteriorly from the postorbital process to the anterior end of the
sagittal crest and correspond to ridges in similar position in
_Thrinaxodon_.

The supraoccipital crest flares upward to a considerable extent in
_Thrinaxodon_ and slopes posteriorly from the skull-roof proper. The
crest extends on either side downward to its confluence with the
zygomatic bar. The area of the crest that is associated with the
temporal musculature is similarly shaped in _Didelphis_.

The zygomatic bar in each genus is stout, laterally compressed, and
dorsally convex on both upper and lower margins. At the back of the
orbit of _Thrinaxodon_, the postorbital process of the jugal extends
posterodorsally. At this position in _Didelphis_, there is but a minor
upward curvature of the margin of the bar.

In _Thrinaxodon_ the dorsal and ventral postorbital processes, arising
from the postorbital and jugal bones respectively, nearly meet but
remain separate. The orbit is not completely walled off from the
adductor chamber. The corresponding processes in _Didelphis_ are
rudimentary so that the confluence of the orbit and the adductor
chamber is complete.

The adductor chamber dorsally occupies slightly less than half of the
total length of the skull of _Thrinaxodon_; in _Didelphis_ the dorsal
length of the chamber is approximately half of the total length of the
skull.

[Illustration: FIG. 7. _Thrinaxodon._ Showing masseter and temporal
muscles. Skull after Romer (1956). Approx. × 7/10.]

The coronoid process in _Thrinaxodon_ sweeps upward posterodorsally at
an angle oblique to the long axis of the ramus. Angular, surangular and
articular bones extend backward beneath and medial to the process. The
process extends above the most dorsal point of the zygomatic bar, as in
_Didelphis_. The mandibular ramus is ventrally convex in both genera.

The relationships described above suggest that _Thrinaxodon_ and the
therapsids having similar morphology in the posterior region of the
skull possessed a temporal adductor mass that was split into major
medial and lateral components (Fig. 7). The more lateral of these, the
masseter, arose from the inner surface and lower margin of the
zygomatic bar and inserted on the lateral surface of the coronoid
process.

The medial division or temporal arose from the sagittal crest and
supraoccipital crest and the intervening dermal roof. The muscle
inserted on the inner and outer surfaces of the coronoid process and
possibly on the bones beneath.

_Thrinaxodon_ represents an advance beyond _Dimetrodon_ in several
respects. The zygomatic bar in _Thrinaxodon_ extends relatively far
forward, is bowed outward and dorsally arched. Consequently, the
masseter was able to extend from an anterodorsal origin to a posterior
and ventral insertion. The curvature of the jaw transforms the
anterodorsal pull of the muscle into a dorsally directed adductive
movement regardless of the initial angle of the jaw. This is the
generalized mammalian condition.

With the development of the secondary palate the area previously
available for the origin of large anterior pterygoid muscles was
reduced. The development of the masseter extending posteroventrally
from an anterior origin presumably paralleled the reduction of the
anterior pterygoids. The therapsid masseter, as an external muscle
unhindered by the crowding of surrounding organs, was readily available
for the many modifications that have been achieved among the mammals.

In the course of synapsid evolution leading to mammals, the temporal
presumably became the main muscle mass acting in adduction of the lower
jaw. Its primacy is reflected in the phyletic expansion of the temporal
openings to permit greater freedom of the muscles during contraction.
In the synapsids that lead to mammals, there is no similar change in
the region of the palate that can be ascribed to the effect of the
pterygoid musculature, even though these adductors, like the temporal,
primitively were subjected to severe limitations of space.


Didelphis

Dissections reveal the following relationships of the external
adductors of the jaw in _Didelphis marsupialis_ (Fig. 8).

     1. MASSETER

     Origin: ventral surface of zygomatic arch.

     Insertion: posteroventral and lateroventral surface of
     mandible.

     2. EXTERNAL TEMPORALIS Origin: sagittal crest; anteriorly
     with internal temporalis from frontal bone; posteriorly with
     internal temporalis from interparietal bone.

     Insertion: lateral surface of coronoid process of mandible.

     3. INTERNAL TEMPORALIS

     Origin: sagittal crest and skull roof, including posterior
     two-thirds of frontal bone, whole of parietal, and
     dorsalmost portions of squamosal and alisphenoid.

     Insertion: medial surface of coronoid process; dorsal edge
     of coronoid process.

[Illustration: FIG. 8. _Didelphis marsupialis._ Showing masseter and
temporal muscles. Skull KU 3780, 1 mi. N Lawrence, Douglas Co., Kansas.
× 3/5.]


Temporal Openings

In discussions of the morphology and functions of the adductor
mechanism of the lower jaw, the problem of accounting for the
appearance of temporal openings in the skull is often encountered. Two
patterns of explanation have evolved. The first has been the attempt to
ascribe to the constant action of the same selective force the openings
from their inception in primitive members of a phyletic line to their
fullest expression in terminal members. According to this theory, for
example, the synapsid opening appeared _originally_ to allow freer
expansion of the adductor muscles of the jaw during contraction, and
continued selection for that character caused the openings to expand
until the ultimately derived therapsid or mammalian condition was
achieved.

The second course has been the attempt to explain the appearance of
temporal openings in whatever line in which they occurred by the action
of the same constant selective force. According to the reasoning of
this theory, temporal fenestration in all groups was due to the need
to decrease the total weight of the skull, and selection in all those
groups where temporal fenestration occurs was to further that end.

Both of these routes of inquiry are inadequate. If modern views of
selection are applied to the problem of explaining the appearance of
temporal fenestrae, the possibility cannot be ignored that:

     1. Selective pressures causing the inception of temporal
     fenestrae differed from those causing the continued
     expansion of the fenestrae.

     2. The selective pressures both for the inception and
     continued expansion of the fenestrae differed from group to
     group.

     3. Selection perhaps involved multiple pressures operating
     concurrently.

     4. Because of different genotypes the potential of the
     temporal region to respond to selective demands varied from
     group to group.

[Illustration: FIG. 9. _Captorhinus._ Diagram, showing some
hypothetical lines of stress. Approx. × 1.]

[Illustration: FIG. 10. _Captorhinus._ Diagram, showing areas of
internal thickening. Approx. × 1.]

[Illustration: FIG. 11. _Captorhinus._ Diagram, showing orientation of
sculpture. Approx. × 1.]

Secondly, the vectors of mechanical force associated with the temporal
region are complex (Fig. 9). Presumably it was toward a more efficient
mechanism to withstand these that selection on the cheek region was
operating. The simpler and more readily analyzed of these forces are:

     1. The force exerted by the weight of the skull anterior to
     the cheek and the distribution of that weight depending
     upon, for example, the length of the snout in relation to
     its width, and the density of the bone.

     2. The weight of the jaw pulling down on the suspensorium
     when the jaw is at rest and the compression against the
     suspensorium when the jaw is adducted; the distribution of
     these stresses depending upon the length and breadth of the
     snout, the rigidity of the anterior symphysis, and the
     extent of the quadrate-articular joint.

     3. The magnitude and extent of the vectors of force
     transmitted through the occiput from the articulation with
     the vertebral column and from the pull of the axial
     musculature.

     4. The downward pull on the skull-roof by the adductor
     muscles of the mandible.

     5. The lateral push exerted against the cheek by the
     expansion of the mandibular adductors during contraction.

     6. The necessity to compensate for the weakness in the skull
     caused by the orbits, particularly in those kinds of
     primitive tetrapods in which the orbits are large.

The distribution of these stresses is further complicated and modified
by such factors as:

     1. The completeness or incompleteness of the occiput and the
     location and extent of its attachment to the dermal roof.

     2. The size and rigidity of the braincase and palate, and
     the extent and rigidity of their contact with the skull.

The stresses applied to the cheek fall into two groups. The first
includes all of those stresses that ran through and parallel to the
plane of the cheek initially. The weight of the jaw and snout, the pull
of the axial musculature, and the necessity to provide firm anchorage
for the teeth created stresses that acted in this manner. The second
group comprises those stresses that were applied initially at an
oblique angle to the cheek and not parallel to its plane. Within this
group are the stresses created by the adductors of the jaw, pulling
down and medially from the roof, and sometimes, during contraction,
pushing out against the cheek.

It is reasonable to assume that the vectors of these stresses were
concentrated at the loci of their origin. For example, the effect of
the forces created by the articulation of the jaw upon the skull was
concentrated at the joint between the quadrate, quadratojugal, and
squamosal bones. From this relatively restricted area, the stresses
radiated out over the temporal region. Similarly, the stresses
transmitted by the occiput radiated over the cheek from the points of
articulation of the dermal roof with the occipital plate. In both of
these examples, the vectors paralleled the plane of the cheek bones.
Similar radiation from a restricted area, but of a secondary nature,
resulted from stresses applied obliquely to the plane of the cheek. The
initial stresses caused by the adductors of the jaw resulted from
muscles pulling away from the skull-roof; secondary stresses, created
at the origins of these muscles, radiated out over the cheek, parallel
to its plane.

The result of the summation of all of those vectors was a complex grid
of intersecting lines of force passing in many directions both
parallel to the plane of the cheek and at the perpendicular or at an
angle oblique to the perpendicular to the plane of the cheek.

Complexities are infused into this analysis with the division of
relatively undifferentiated muscles into subordinate groups. The
differentiation of the muscles was related to changing food habits,
increased mobility of the head, and increase in the freedom of movement
of the shoulder girdle and forelimbs (Olson, 1961:214). As Olson has
pointed out, this further localized the stresses to which the bone was
subjected. Additional localization of stresses was created with the
origin and development of tetrapods (reptiles) that were independent of
an aquatic environment and were subjected to greater effects of gravity
and loss of bouyancy in the migration from the aqueous environment to
the environment of air. The localization of these stresses was in the
border area of the cheek, away from its center.

What evidence is available to support this analysis of hypothetical
forces transmitted through the fully-roofed skull of such an animal as
_Captorhinus_?

It is axiomatic that bones or parts of bones that are subject to
increased stress become thicker, at least in part. This occurs
ontogenetically, and it occurs phylogenetically through selection. Weak
bones will not be selected for. Figure 10 illustrates the pattern of
the areas of the skull-roof in the temporal region that are marked on
the internal surface by broad, low thickened ridges. The position of
these ridges correlates well with the position of the oriented stresses
that were presumably applied to the skull of _Captorhinus_ during life.
It can be seen from Figure 10 that the central area of the cheek is
thinner than parts of the cheek that border the central area. The
thickened border areas were the regions of the cheek that were
subjected to greater stress than the thin central areas.

External evidence of stress may also be present. The pattern of
sculpturing of _Captorhinus_ is presented in Figure 11. The longer
ridges are arranged in a definite pattern. Their position and direction
correlates well with the thickened border of the cheek, the region in
which the stresses are distinctly oriented. For example, a ridge is
present on the internal surface of the squamosal along its dorsal
border. Externally, the sculptured ridges are long and roughly
parallel, both to each other and to the internal ridge.

The central area of the cheek is characterized by a reticulate pattern
of short ridges, without apparent orientation. The thinness of the bone
in this area indicates that stresses were less severe here. The random
pattern of the sculpture also indicates that the stresses passed in
many directions, parallel to the plane of the cheek and obliquely to
that plane.


_Possible Explanation for the Appearance of Temporal Openings_

Bone has three primary functions: support, protection and participation
in calcium metabolism. Let us assume that the requirements of calcium
metabolism affect the mass of bone that is selected for, but do not
grossly affect the morphology of the bones of that mass. Then selection
operates to meet the needs for support within the limits that are set
by the necessity to provide the protection for vital organs. After the
needs for protection are satisfied, the remaining variable and the one
most effective in determining the morphology of bones is selection for
increased efficiency in meeting stress.

Let us also assume that bone increases in size and/or compactness in
response to selection for meeting demands of increased stress, but is
selected against when requirements for support are reduced or absent.
Selection against bone could only be effective within the limits
prescribed by the requirements for protection and calcium metabolism.

We may therefore assume that there is conservation in selection against
characters having multiple functions. Since bone is an organ system
that plays a multiple role in the vertebrate organism, a change in the
selective pressures that affect one of the roles of bone can only be
effective within the limits set by the other roles. For example,
selection against bone that is no longer essential for support can
occur only so long as the metabolic and protective needs of the
organism provided by that character are not compromised. If a character
no longer has a positive survival value and is not linked with a
character that does have a positive survival value, then the metabolic
demands for the development and maintenance of that character no longer
have a positive survival value. A useless burden of metabolic demands
is placed upon the organism because the character no longer aids the
survival of the organism. If selection caused, for example, muscles to
migrate away from the center of the cheek, the bone that had previously
provided support for these muscles would have lost one of its
functions. If in a population of such individuals, variation in the
thickness of the bone of the cheek occurred, those with thinner bone in
the cheek would be selected for, because less metabolic activity was
diverted to building and maintaining what is now a character of reduced
functional significance. A continuation of the process would eliminate
the bone or part of the bone in question while increasing the metabolic
efficiency of the organism. The bone is no longer essential for
support, the contribution of the mass of bone to calcium metabolism and
the contribution of this part of the skeleton to protection have not
been compromised, and the available energy can be diverted to other
needs.

The study of _Captorhinus_ has indicated that the central area of the
cheek was subjected to less stress than the border areas. A similar
condition in basal reptiles may well have been present. A continued
trend in reducing the thickness of the bone of the cheek in the manner
described above may well have resulted in the appearance of the first
reptiles with temporal fenestrae arising from the basal stock.

Such an explanation adequately accounts for an increased selective
advantage in the step-by-step thinning of the cheek-wall prior to the
time of actual breakthrough. It is difficult to see the advantage
during such stages if explanations of weight reduction or bulging
musculature are accepted.

After the appearance of temporal fenestrae, selection for the classical
factors is quite acceptable to explain the further development of
fenestration. The continued enlargement of the temporal fenestrae in
the pelycosaur-therapsid lineage undoubtedly was correlated with the
advantages accrued from securing greater space to allow increased
lateral expansion of contracting mandibular adductors. Similarly,
weight in absolute terms can reasonably be suggested to explain the
dramatic fenestration in the skeletons of many large dinosaurs.


Literature Cited

ADAMS, L. A.

     1919. Memoir on the phylogeny of the jaw muscles in recent
           and fossil vertebrates. Annals N. Y. Acad. Sci.,
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ESTES, R.

     1961. Cranial anatomy of the cynodont reptile _Thrinaxodon
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HOTTON, N.

     1960. The chorda tympani and middle ear as guides to origin
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OLSON, E. C.

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ROMER, A. S.

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     1956. Osteology of the reptiles. Univ. Chicago Press, xxii +
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ROMER, A. S. and PRICE, L. I.

     1940. Review of the Pelycosauria. Geol. Soc. Amer. Special
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WATSON, D. M. S.

     1948. _Dicynodon_ and its allies. Proc. Zool. Soc. London,
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     _Transmitted December 5, 1963._


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