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.

[Ill.u.s.tration: FIG. 9. _Captorhinus._ Diagram, showing some hypothetical lines of stress. Approx. 1.]

[Ill.u.s.tration: FIG. 10. _Captorhinus._ Diagram, showing areas of internal thickening. Approx. 1.]

[Ill.u.s.tration: FIG. 11. _Captorhinus._ Diagram, showing orientation of sculpture. Approx. 1.]

Secondly, the vectors of mechanical force a.s.sociated 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 a.n.a.lyzed 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 a.s.sume 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 pa.s.sing 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 a.n.a.lysis 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 a.n.a.lysis 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 ill.u.s.trates 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 pa.s.sed 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 partic.i.p.ation in calcium metabolism. Let us a.s.sume that the requirements of calcium metabolism affect the ma.s.s of bone that is selected for, but do not grossly affect the morphology of the bones of that ma.s.s. 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 a.s.sume 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 a.s.sume 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 ma.s.s 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 cla.s.sical 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 s.p.a.ce 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., 28:51-166, 8 pls.

ESTES, R.

1961. Cranial anatomy of the cynodont reptile _Thrinaxodon liorhinus_. Bull. Mus. Comp. Zool., 125(6):165-180, 4 figs., 2 pls.

HOTTON, N.

1960. The chorda tympani and middle ear as guides to origin and development of reptiles. Evolution, 14(2):194-211, 4 figs.

OLSON, E. C.

1961. Jaw mechanisms: rhipidistians, amphibians, reptiles.

Am. Zoologist, 1(2):205-215, 7 figs.

ROMER, A. S.