Australia: The Land Where Time Began

A biography of the Australian continent 

Skeletal Changes – Skull and Shoulder Girdle

Of the changes that have occurred in the skull and shoulder girdle some are obvious while others are more subtle, involving changes such as the proportions. When the skull of Eusthenopteron is compared with that of Acanthostega a tetrapod from the Devonian, what is probably the most obvious difference, according to Clack¹, is the bones covering the gill chamber and throat region of fishes, the operculogular series, the tetrapods had lost the entire series. Though it is tempting to believe the loss of the bones was connected with the shift away from gill breathing, reasons have been suggested why this may not necessarily be the case. This was an important change as it occurred in conjunction with a suite of other changes. Clack¹ says that it is beginning to be suggested by new finds which of the changes occurred first, though it is not yet clear which occurred first.

The series of movements that pump water across the gills a fish to allow gas exchange with the water, oxygenating the blood, the opercular series has a key function. This is one of the functions of the skeleton that is transformed in the transition from fish to tetrapod, some of these functions being explained with the aid of an understanding of this mechanism. Movements of the mouth (buccal) chamber and opercular system power the pumping mechanism, the buccal pump. There are distinct phases in its operation during which flexible joints between the roof of the skull and cheeks in ray-finned fishes, as also occurred in lobe-finned fishes, facilitated the expansion of the buccal chamber and the opercular chamber as they expand and contract, and this expansion-contraction cycle of the buccal chamber is slightly out of phase with the that of opercular chamber. Pressure differentials are thereby allowed to exist between the buccal chamber and the opercular chamber, and it is this phase difference that causes the water to flow from the buccal chamber to the opercular chamber and then out to the surrounding water. The breathing by gills was first reduced in the transition to tetrapods and eventually lost completely as the adult metamorphosed into the amphibian, and then to all amniotes. The earliest lungs were ventilated by the buccal pump, the operation of which used the hyoid skeleton, as it does in modern amphibians, though it is eventually taken over by the muscles of the body wall, which then allows the hyoid skeleton to be converted for other uses.

The skull of tetrapods also lacks another series of bones that were present in fishes, as well as losing the opercular series, called the extrascapulars and supracleithrals, which functioned in fishes to join the dermal shoulder girdle to the roof of the skull at the back. The bones at the back of the skull table are the extrascapulars, of which there are usually 3, as was the case in Eusthenopteron, and the supracleithrals are the bones present above the cleithrum in the shoulder girdle. These bones link to one another at the back of the head in Eusthenopteron. A space was made between the suspensorium and the shoulder girdle when the operculogulars, extrascapulars and supracleithrals were lost; in effect the head was no longer supported by the shoulder girdle, the vertebral column and the shoulder muscles taking over the job of the shoulder girdle, with the result that tetrapods have necks.

A number of changes were involved in the construction of the neck, such as the muscles holding the head up require a solid foundation for their origin. Over time the head of tetrapods gradually adapted to provide anchorage and space for the attachment of these muscles. Strong insertion points along the spine were required, and another gradual change that took place in the evolution of tetrapods was elaboration of the neck vertebrae. Some of the muscles that support the head and join it to the vertebral column insert into the posttemporal fossae, which are pockets at the back of the skull. The occiput (neck joint) that is constructed to allow the head to move freely on the vertebral column, is another feature of tetrapods that required gradual changes to the back of the skull and the front of the vertebral column.

The development of the neck also involved changes to the braincase. In fishes the notochord extended through the vertebral column and into the braincase, which aided the body to return to shape following the bending that was produced by the body wall muscles during swimming. The notochord is sheathed by the serially arranged centra in the vertebral column of fishes, extending into the braincase through an opening below the foramen magnum. The notochord has been replaced by bone in each centrum in most tetrapods and no longer enters the braincase. As with the evolution of the neck joint, it is possible to trace this process in the transition from fish to tetrapod because it occurred gradually.

Clack¹ suggests a number of other changes concerning the braincase occurred that may have been associated with this change, one of which is the hinge between the anterior and posterior parts of the braincase that is present in Eusthenopteron. This feature was lost among fishes that were advanced and tetrapod-like, according to most current estimates of phylogeny of these animals. In fishes, the dermal parasphenoid bone lies beneath only the anterior (ethmosphenoid) part of the braincase. In tetrapods the elongation of the dermal parasphenoid sealed the former hinge line by extending to underlie both the anterior and posterior parts of the skull. The former hinge along the roof of the skull was also eliminated in tetrapods, and this is seen when the dorsal views of the skulls of Eusthenopteron and Acanthostega are compared.

There are a number of changes that took place in the part of the skull behind the eyes. The posterior portion of the skull of fishes is generally longer than the same portion of the skulls of early tetrapods, in both the braincase and the roof of the skull. According to Clack¹ when a series of tetrapod skulls from the Devonian to the Permian in chronological order are compared it can be seen that there is a trend in skull shortening at the back.  The otic capsule, located beneath the skull table, appears to be the reason for this shortening, because in tetrapods, relative to the remainder of the skull, it becomes gradually smaller compared to the condition in fishes. This trend began in very early tetrapods, though the reason is unclear.

It is suggested that one of the more mysterious changes that occurred in braincase may possibly have been associated with the otic region shortening. In most fishes the point where the hyomandibula attached to the otic capsule, the lateral commissure in Eusthenopteron, was lost in tetrapods. The cavity that resulted was eventually occupied by the head of the hyomandibula, inserting instead into the sidewall of the braincase. The bone is known as a stapes at this point and the fenestra vestibule is the hole into which it inserts.

The hyomandibula of fishes has a number of functions. It is a long, flattened bone with its articulation on the wall of the braincase from where it extends down the back of the palatoquadrate and supports the bones from the roof of the mouth. In order to accommodate the expansion and contraction of the buccal cavity during the breathing cycle of the fish, and in the movements of the feeding mechanism, the mouth roof needs to be moveable, these movements being controlled by the hyomandibula. The hyomandibula also coordinates the movements of the operculogular series, the gill covers, that the hyomandibula is attached to, that also operate during the breathing cycle, with those of the palate. There are also other points at which the palatoquadrate joins to the braincase: at the front and around the middle of its length at the basal articulation, though these bones are all mobile. Therefore, in fishes the palatal bones are attached loosely to the braincase, mostly through the hyomandibula, this skull type being described as hyostylic.

This type of flexible skull construction was eliminated in the later tetrapods, with the joints becoming firm and sutured together. The palate has its own firm attachments to the braincase and the bones of the roof of the skull; therefore it does not need to be hung from the hyomandibula. Clack¹ suggests this may be one of the reasons the stapes in tetrapods is so much smaller than the hyomandibula of fishes. Tetrapods that have this type of skull construction are termed autostylic. The hyomandibula assumed a different role in tetrapods as a hearing ossicle. This change in role occurred in a series of steps over an extended period of time.

According to Clack¹ this change is associated with changes that took place in the branchial system. Eventually, tetrapods completely lost the ability to breath by gills, the gill arches becoming reduced in both size and number, though without the loss of the bones supporting the gill arches or the muscles that moved them, which were redeployed as tongue supports and musculature. When tetrapods became terrestrially feeding animals they could no longer use water to support food while they grasped it, or use the density of water in suction feeding as is used by many fish. The tetrapods developed the grasping and manipulating tongue, a unique tetrapod feature that was constructed from what were former components of gill arches. It is suggested this could probably occur only once the breathing by gills had been entirely abandoned, which may explain why such different tongue operational mechanisms from those of amniotes are used by modern amphibians, as the juvenile amphibians have retained the gill method of breathing.

The spiracle opened into the apex of a slot called the spiracular notch or cleft at the back of the skull in fish such as Eusthenopteron. In most tetrapods, though not all, there was a rounded or V-shaped embayment at the same location in the skull variously called the otic notch, the spiracular notch, and the temporal notch, the function of this embayment being debated by palaeontologists for a long time. Clack¹ says the story behind it is connected with the change from gill breathing to air breathing and in the form and function of the hyomandibula/stapes.

Though in tetrapods the back of the skull was generally shorter than it was in comparable fish, the snout appears to have grown longer with the result that the eyes appeared to be further back on the head. More of the tooth row came to be in front of the eyes as a result of this extension of the snout in tetrapods than its position in fish. There also appears to have been a move of the eyes closer to the top of the head in the early tetrapods and was the case in the fishes. It is difficult to explain changes such as these and it is hard to separate them from each other. They may be linked to changes that had occurred with both sensory and feeding requirements.

It appears snout lengthening may have been associated with the stabilisation of the bone pattern in the forward part of the skull as well as a reduction in the number of bones. Tetrapods had evolved a single pair of nasal bones, the remnants of the many small bones as found in fish being present only in the earliest tetrapods, while in the nasal region fishes had a mosaic of small bones. The lateral and median rostrals and anterior tectal bones of fishes were lost early in the history of tetrapods.

There were other changes that were more subtle, e.g., changes to the cheekbones, the internal and external nostrils, the spiracular notch, the dentition, and the lateral line, which was the aquatic sensory system, all of which took place during the transition from fish to tetrapod. These are best seen in the study of particular fishes and tetrapods in context.

The shoulder girdle underwent profound changes during the transition, which were associated with a change in the emphasis of the role played by the complex. The shoulder girdle is integral with the skull in fishes and continuing the profile of the skull back along the body in a smooth line which produced the hydrodynamic torpedo shape that is typical of many fishes. It mainly consists of dermal elements, the supracleithral bones, the cleithrum, the clavicle and a small ventral midline interclavicle. The series of bones that forms a hoop around the body attaches to the skull at the top by the lateral extrascapular bones. Muscles extend from the midline of the shoulder girdle to the gill arches and jaws, under the body, to control their movements. A groove and internal flange called the postbranchial lamina along the anterior of the cleithrum and clavicle, not only to help direct water flow out of the gill chamber, also helping to form a seal which the operculum closes against during the movements of breathing.

On the inner surface of the cleithrum a small endochondral scapulocorocoid is wedged, bearing a small articulation point, which is backwardly facing, for the fin. In Eusthenopteron the scapulocorocoid is a small tripod of bone, the 3 “legs” of which are attached to the cleithrum.

In all but the most primitive of the tetrapods the shoulder girdle consists mainly of an enlarged scapulocoracoid, which may be divided into 2 or 3 ossifications lather in the evolution of the tetrapods: the scapula above, and 1 or 2 coracoids below. A slender dermal cleithrum clasps along the scapular portion’s anterior margin, though this is also lost later in the evolution of tetrapods, the clavicle remaining in most tetrapods. In the early tetrapods it consists of a broad triangular ventral plate with an apex positioned at the side of the body, which is produced into a prong that is upwardly projecting. The coracoid portion of the girdle is sheathed by this and contacts the slender cleithrum. The dermal interclavicle may be a large plate of bone that is shield-shaped, or it can be a T-shaped one that is more slender, though in early tetrapods it is always larger than the corresponding bone in fishes. In tetrapods the scapulocoracoid bears a large concave articulation surface for the limb which faces outwards from the body.

In fishes the shoulder girdle mainly functions in hydrodynamics, though it also provides anchorage for the muscles that move the gills and jaws. The bearing of the pectoral fins appears to be a relatively minor role, but in the tetrapods, where the pectoral fins are replaced by the limbs, the provision of an anchorage for the muscles that move them has assumed a more important function. The limbs and head in tetrapods are allowed greater movement than in fishes by the shoulder girdle being detached from the skull. The outer dermal components are correspondingly larger in fishes, though in tetrapods they are reduced in favour of the inner endochondral elements. In the earliest tetrapods the shoulder girdles do not have a structure that is halfway between those of fishes and those of the later tetrapods, rather, they have some characters that are unique and some that are unexpected.

Sources & Further reading

1. Clack, Jennifer A., 2012, Gaining Ground: The Origin and Evolution of Tetrapods, 2nd. Edition, Indiana University Press