The development of the branchial region in vertebrates is no less dependent on the cooperation of parts of different origin than is the mouth region. The leading part in the development of this area belongs to the endoderm. The endodermal cavity in this region, from its beginning, is distended in a transverse direction.
In amphibians it is derived from the inflated part of the foregut. In the stage immediately following the closure of the neural tube, the lateral walls of the pharyngeal cavity bulge out and produce a series of outwardly directed pockets on each side. These pockets are the pharyngeal pouches or branchial pouches.
The pharyngeal pouches are developed one after another, beginning with the first pair, that is, the one lying just posterior to the mandibular arch. As the endodermal pharyngeal pouches reach the epidermis, having pushed aside the intervening mesoderm, the epidermis folds inward to meet the pharyngeal pouches.
A series of branchial grooves is thus developed on the surface of the embryo, each groove corresponding to an endodermal pouch. The outer wall of the endodermal pouch and the inner wall of the epidermal groove fuse into a branchial membrane, similar to the oropharyngeal membrane.
A gill cleft is formed when the branchial membrane becomes perforated, so that an open communication is established between the pharyngeal cavity and the outer medium. In aquatic vertebrates gill filaments are then developed on the walls of the gill clefts. These filaments are the internal gills.
The development does not always reach the final stage (the formation of the gill filaments serving for respiration). Even in aquatic vertebrates, some of the pharyngeal pouches may not develop into gill clefts. Thus, in bony fishes and amphibians, the first pair of pharyngeal pouches (the one lying behind the mandibular arch) does not reach the epidermis and remains a blind diverticulum of the pharyngeal wall.
In the amniotes, the gills never function as respiratory organs, but four pairs of pharyngeal pouches nevertheless develop. Branchial grooves and branchial membranes are formed, and in the first three pairs of pharyngeal pouches the branchial membranes are broken so that gill clefts are formed. The fourth pouch does not open to the outside.
The existence of open gill clefts is, however, of very short duration, and the clefts are again closed by membranes. The new closing membranes develop farther out than the original branchial membranes and are produced as folds of ectoderm only, whereas the original branchial membranes consisted of a layer of ectoderm on the outside and endoderm on the inside.
The whole system is later reduced to a greater or lesser extent, and its remnants are used up for the development of parts having nothing to do with the respiratory function. Thus, the first pair of pharyngeal pouches becomes the Eustachian tube in the terrestrial vertebrates. The third and fourth pharyngeal pouches give rise to a series of glands of internal secretion, the thymus and the parathyroids.
These organ rudiments develop from masses of cells that become detached from the walls of the pharyngeal pouches and are then shifted downward and backward until they come to lie in the neck or in the anterior trunk region. The main part of the thymus is derived from the third pair of pharyngeal pouches.
The pouches actually become extended lateroventrally, and this extension is later used in the formation of the thymus rudiment. Its development is of great importance, as it is now known that the lymphocytes which in higher vertebrates and in man perform the cell-mediated immune responses are differentiated exclusively in the thymus.
It has been generally believed that the cells giving rise to the parathyroid glands and the thymus are derived from the endodermal part of the pharyngeal pouches. There are indications, however, that at least part of the thymus rudiment is derived from the ectodermal cells of the branchial grooves. The importance of these glands for the well-being of the animal may account for the persistence of the branchial pouches in the embryos of terrestrial animals, although they have long since lost their original functional significance.
Another important gland of internal secretion associated with the pharynx in its development is the thyroid gland. The thyroid gland develops in vertebrates as a ventral pocket in the floor of the pharynx. Subsequently the pocket becomes closed and separated from the pharyngeal wall. The thyroid rudiment is then displaced in a caudal direction, until in terrestrial vertebrates; it comes to lie ventral to the trachea.
It has already been stated that the endodermal pharyngeal pouches are the initiators of all the developments in the branchial region. The epidermal branchial grooves are induced by the endodermal pouches when they touch the epidermis. Without the endodermal pharyngeal pouches, the epidermal grooves do not develop, nor do they develop if the endodermal pouch, though present, does not reach the epidermis (as in the case of the first pouch in amphibians and bony fishes).
For the development of the external gills in the urodeles, it is also necessary that the endodermal pharyngeal pouch reach the epidermis; otherwise, the gills fail to appear. The external gills in the urodeles are later supplemented by internal gills- gill filaments developing on the branchial arches.
Both external and internal gills function simultaneously, until both are reduced during metamorphosis. In the anurans, the external gills function only temporarily, during a short period after the hatching of the larvae. Soon after the small tadpoles begin to swim, a fold of skin, the opercular fold, appears anterior to the external gills. The opercular fold spreads backward over the gill region, covering both the external gills and the gill slits.
Both are thus included in a branchial cavity. The posterior edge of the opercular fold becomes attached to the skin behind the branchial region, so that only a narrow opening, the branchial aperture, leads from the branchial cavity to the exterior. At the same time, the external gills are reduced in size, and the internal gills develop on the branchial arches beneath the external gills and function throughout the whole period of larval development.
The visceral skeleton is an important integral part of the branchial region. The visceral skeleton develops from cells of the neural crest. In their downward migration, these cells are split by the pharyngeal pouches into several streams, moving in between the adjacent pharyngeal pouches.
Later, the branchial arches are formed by the chondrification of the neural crest mesenchyme in about the same position as the masses of migrating cells were to be found. The dependence of visceral arch development on the gill clefts is, however, a more intimate one than would follow from this description. In the absence of the pharyngeal pouches, the neural crest mesenchyme does not chondrify, and no branchial arches are formed.
If the number of pharyngeal pouches is reduced (after an operation in which part of the endoderm of the branchial region has been removed), the number of visceral arches is similarly reduced; one skeletal arch is developed on each side of the remaining pharyngeal pouches. Thus, the number of arches is one more than the number of pouches present. The hyoid arch shows the same kind of dependence on the pharyngeal pouches as the branchial arches proper.
For the development of the visceral arches, it is not necessary for the endodermal pharyngeal pouches to establish a connection with the epidermis and for the gill cleft to break through. The presence of the endodermal pouches, even if they are represented by blind pockets, is sufficient to induce the development of the skeletal arches.
We can now review the dependence of the development of the various parts of the visceral skeleton on the adjoining parts of the alimentary canal:
1. The upper part of the mandibular arch (the quadrate and the region of articulation with the lower jaw) develops independently of parts of the alimentary canal.
2. The lower part of the mandibular arch is dependent on the ectodermal mouth invagination.
3. The hyoid arch and the branchial arches are dependent on the endodermal pharyngeal pouches.
A very peculiar feature in the development of the amphibian visceral skeleton is presented by the second basibranchial. The skeletal element is developed from mesodermal mesenchyme, not from neural crest mesenchyme, and it is also independent of the endodermal pharyngeal pouches. It is formed even if the whole of the endoderm of the branchial region has been removed.
The visceral arches, which are dependent in their development on the epithelial parts of the alimentary canal, appear to exercise some influence on the development of the teeth. The tooth rudiments, consisting of the ectodermal or endodermal enamel organ and the papilla, derived from neural crest mesenchyme, are formed in connection with certain skeletal elements – Meckel’s cartilage, the rudiments of the vomer and palatine bone, and later the rudiments of the pre-maxilla, maxilla, and dental bone.
With the reduction of the pharyngeal pouches in adult terrestrial vertebrates, the visceral skeleton becomes modified. The lower end of the hyoid arch persists as the body of the hyoid bone, and the lower part of the first branchial arch is utilized in the formation of the horns of the hyoid bone. Parts of the subsequent branchial cartilages contribute to the formation of the thyroid cartilages and the cartilages surrounding the trachea.