Archenteron & Alimentary Canal in Vertebrates | Endodermal Organs | Embryology

The relation between the archenteron and the definitive alimentary canal is very different in vertebrates with complete cleavage from that in vertebrates with incomplete (meroblastic) cleavage.

The Relation in Lower Vertebrates:

The archenteron in Amphioxus is originally lined with presumptive endoderm, presumptive mesoderm, and presumptive notochordal cells. When the notochord and the mesoderm are segregated from the endoderm, the latter closes the gap on its dorsal side, and the resulting cavity becomes the cavity of the alimentary canal.

In holoblastic vertebrates—cyclostomes, ganoid fishes, lungfishes, and amphibians—the presumptive notochord and mesoderm also participate in the lining of the archenteron, forming its roof. This roof is segregated from the endoderm and the endodermal cavity which is closed by the fusion of the free edges of the endodermal layer.

The resulting endodermal cavity consists of three unequal portions. The anterior portion is dilated and lined by a relatively thin endodermal epithelium. This part is usually referred to as the foregut. The following portion is called the mid-gut. The cavity of the mid-gut is narrower.

Dorsally it is lined by a rather thin epithelium, but the ventral wall consists of a mass of large cells containing abundant yolk, so that the wall here is very thick. The most posterior part of the cavity which adjoins the blastopore may be distinguished as the hindgut.

The fate of the various parts of the endodermal lining of the fore- and mid-gut in amphibians has been elucidated by the method of local vital staining. To stain the inner surface of the gut, cuts were made through the body wall (in some experiments through the neural plate), and pieces of agar soaked in vital stain were applied to the endoderm from the inside. After the stain was taken up by the endodermal cells, the agar was removed. The wound healed easily, and the embryos continued to develop apparently quite normally.

In the neurula stage, the ventral wall of the foregut becomes flattened out and later even folded slightly upward. The cavity is thus subdivided into two pocket-like recesses. The larger anterior one, lying immediately underneath the brain, gives rise to the cavities of the mouth and of the branchial region.

The posterior pocket, bordering on the mass of yolk-laden cells of the mid-gut, is known as the liver diverticulum (or hepatic diver­ticulum) although in addition to giving rise to the rudiments of the liver and the pancreas it also participates in the formation of the stomach and the duodenum.

It is rather remarkable that in frogs the liver diverticulum is extended downward and backward until the endoderm is perforated, and the gut cavity opens into the space between the endoderm and mesoderm on the ventral side of the embryo. The significance of this perforation is not known.

The liver diverticulum becomes extended as a funnel-shaped invagination farther and farther in a posteroventral direction, drawing into it the rudiments which were originally located in the walls of the broadened cavity of the foregut (such as the rudiments of the anterior part of the duodenum, stomach, and esophagus).

These rudiments become reshaped in the form of a narrow tube. This transformation can best be shown by considering the development of the stomach in the frog embryo. In the neurula stage, the presumptive material of the stomach is arranged in the form of a narrow ring, the ventral part of which lies just in front of the liver diverticulum, the dorsal part occupies the roof of the gut just at the mouth of the mid-gut, and the right and left parts obliquely cross the lateral walls of the foregut.

This ring contracts and at the same time broadens until eventually the rudiment of the stomach becomes more or less barrel-shaped, with a fairly narrow cavity. The tube is constricted to an extreme degree between the pharynx and the stomach and may even be temporarily occluded in this region, which becomes the rudiment of the esophagus, a very short section of the gut in the embryo.

The part of the gut in front of the stomach rudiment also elongates, but instead of becoming tubular it is flattened dorsoventrally and expanded sideways. Most of this cavity becomes the pharynx. The floor of the pharynx is raised, partially as a result of the increase of the heart rudiment, which develops just underneath.

The lateral edges of the pharynx are drawn outward even more and form the pharyngeal pouches. The epithelium lining the pharynx becomes rather thin, in contrast to the lining of the rest of the alimentary canal.

The part of the liver diverticulum posterior to the stomach retains a fairly broad cavity. At the same time, the cavity of the mid-gut (in urodeles and in most frogs) becomes occluded by the yolky endodermal cells. For a time there is no cavity in the mid-gut, and the gut cavity ends with the liver diverticulum.

Subsequently, the centrally lying yolky cells of the mid-gut break down and become resorbed, and the remaining cells are rearranged around a new cavity which extends in a posterior direction from the liver diverticulum. The liver diverticulum thus becomes incorporated into the main channel of the alimentary canal.

This mode of development of the alimentary canal of the amphibians was first described for urodeles, and the findings were confirmed in all essential points by work done on frogs. In some frogs, however, such as Xenopus laevis, the mid-gut cavity is not completely closed at any stage and later expands to form the intestinal cavity.

At the time when the mid-gut becomes occluded, the hindgut does not lose its cavity, and the latter persists as the cavity of the cloaca. The dorsal wall of the hindgut becomes extended into the tail rudiment as a postanal gut. The postanal gut has only an ephemeral existence and is soon broken up and disappears. The hindgut also gives rise in amphibians to the urinary bladder, which develops as a ventral evagination of the gut in late stages of larval life.

As the main portions of the alimentary canal begin to take shape, the canal as a whole becomes twisted in a characteristic way. At an early stage, the stomach has already assumed a slanting position. Subsequently, the posterior end of the stomach is shifted to the left, while the adjoining part of the duodenum comes to lie transversely, going from left to right.

The distal part of the duodenum is then bent in such a way that it leads to the anterior end of the intestine, which is more or less in a dorsal position. The alimentary canal thus performs a complete spiral revolution, which may be referred to as the gastroduodenal loop and which occurs with greater or lesser modifications in all vertebrates.

Where the loop is in its lowest position, it leaves a space or saddle on the dorsal side, and this space is taken up by the rudiment of the pancreas. The posterior part of the alimentary canal also becomes twisted into folds and loops as a result of the elongation of the alimentary canal which exceeds the elongation of the body.

The folding and twisting of the duodenum and intestine are especially prominent in the tadpoles of frogs which, in connection with their herbivorous diet, have a very long intestine. The pattern of twisting varies somewhat in different frogs and need not be considered here. In urodeles and also in fishes, the intestine does not elongate to the same degree, and its folding may be very limited, though the gastroduodenal loop is always present.

The Relation in Higher Vertebrates:

In vertebrates having a meroblastic type of cleavage, the development of the alimentary canal presents very different problems, and the processes leading to the formation of the definitive cavity of the alimentary canal are quite peculiar. 

It must be noted in the first instance that in birds the archenteric cavity is often lacking altogether, and if it is present, as a canal leading forward from Hensen’s node, it is very small and its walls are not endodermal. The starting point for the development of the alimentary canal proper is a sheet of endoderm lying flat under the ectodermal and mesodermal parts of the embryonic region of the blastodisc.

The sheet of endoderm lies flat on the yolk of the yolk sac or forms the roof of the mammalian yolk sac, which is a space filled with fluid. In both cases, the cavity of the alimentary canal is separated from the cavity of the yolk sac by a process of infolding.

During this infolding, the median strip of the endoderm lying immediately under the notochord and somites remains in this position, while the immediately adjoining strips on the right and left become inflected downward, and the crests of the folds converge toward the middle and eventually fuse. The inner surfaces of the folds contribute to the formation of the floor of the gut, while the outer surfaces of the folds are continuous with the endodermal lining of the yolk sac.

Concurrently with the movement of the endodermal layer in a transverse plane, a complicated shifting has been found to occur longitudinally. The median strip which forms the dorsal wall of the gut slides forward, while in the folds closing the gut laterally and ventrally, endodermal material moves obliquely backward.

During their movement downward, the lateral strips of endoderm are accompanied by the visceral layer of the lateral plate mesoderm, which closely adheres to the endoderm throughout this whole series of formative movements. It is probable that the dynamic force of the movement is due to the endoderm and mesoderm jointly.

As a result of the downward movement of the visceral layer of the lateral mesoderm, the coelomic cavity becomes considerably expanded locally. The coelom is reduced again, however, when the body folds undercut the embryo. The alimentary canal becomes separated from the yolk sac cavity initially at the anterior end of the embryo. This part corresponds to the foregut of the amphibian embryo.

Somewhat later, the posterior part of the endodermal groove closes into a canal that becomes the posterior part of the alimentary system, which in the amniotes is called the hindgut, although most of it corresponds to the mid-gut of amphibian embryos. Between the foregut and the hindgut a gap remains where the endoderm does not close to form a canal, or even a groove, and where it is in open communication with the yolk sac. This part, in amniotes, is referred to as the mid-gut.

Where the edges of the folds separating the foregut from the yolk sac meet in the middle they form a ridge, known as the anterior intestinal portal. A similar edge at the anterior end of the hindgut is the posterior intestinal portal. The gap between the two is very large at first, but its relative size diminishes with the growth of the embryo, and eventually it is reduced to the opening of the yolk stalk, connecting the gut cavity to the cavity of the yolk sac.

From the beginning the foregut is much broader than the hindgut and is flattened in cross section. As in amphibians, the foregut gives rise to the endodermal lining of all anterior parts of the alimentary canal, including most of the duodenum, the liver, and pancreas developing just in front of the anterior intestinal portal.

The oral and especially the pharyngeal parts of the foregut remain expanded in a transverse direction, and the pharynx becomes drawn out to form the pharyngeal pouches, but the posterior part of the foregut, corresponding to the esophageal, gastric, and duodenal parts of the alimentary canal, eventually becomes round in cross section.

The esophagus in higher vertebrates is soon greatly elongated, in connection with the development of the neck. The hindgut is, from the start, narrower than the foregut and soon also becomes round in cross section.

Although the foregut in higher vertebrates is quite different in shape from the foregut of amphibians, it develops the gastroduodenal loop in much the same way. The anterior (cardiac) end of the stomach is displaced to the left side, and the posterior (pyloric) end is turned downward and toward the middle, while the anterior part of the duodenum assumes a transverse direction, thus bringing about the familiar position of the stomach in adult mammals and birds.

The intestine becomes convoluted in a pattern that varies greatly not only between different classes but even within one class, such as in various mammals. A peculiarity occurring in mammals is that sections of the intestine adjoining the yolk stalk, both anteriorly and posteriorly, sink down into the umbilical cord and lie for a time practically outside the body of the embryo proper as a sort of umbilical hernia.

The convolutions of the intestine begin forming inside the umbilical cord, but well before birth the definitive intestine is withdrawn into the body, and only the yolk stalk remains in the cord. (This occurs in the human embryo during the third month of pregnancy.)

The posterior end of the hindgut gives rise to the cloaca and also to a postanal gut, which disappears later. The ventral wall of the cloaca produces the allantoic diver­ticulum (the endodermal part of the allantois).

In higher mammals (in particular in man), however, the allantoic diverticulum is formed very early as an outgrowth of the yolk sac at the posterior end of the embryo, even before the embryo becomes subdivided into the embryonic body and the extra-em­bryonic parts. Later, the allantoic diverticulum is incorporated into the ventral floor of the mid-gut and assumes the same position that it has in lower amniotes.

At the time of their formation, both the foregut and the hindgut are blind diverticula, without openings to the exterior at the front and hind ends of the embryo. The formation of the mouth opening at the anterior end of the foregut occurs in much the same way in both holoblastic and meroblastic vertebrates.

The development of the anal or cloacal opening, however, is different in the two types of vertebrates. In some vertebrates with holoblastic cleavage, the blasto­pore (or part of it) persists as the anal (cloacal) opening. In others the anus is formed early in embryonic life near the spot where the blastopore opening had been.

As, in higher vertebrates, there is no patent blastopore leading into an endodermal archenteron, the cloacal opening has to develop by a perforation of the body wall at the posterior end of the hindgut. The point at which this perforation occurs is discernible as early as the primitive streak stage and lies at the posterior end of the streak.

When the primitive streak shrinks in the late gastrulation stages, it leaves in front the three germinal layers – the ectoderm, the mesoderm, and the endoderm, lying one above the other. At the posterior end, however, the separation of germinal layers does not occur; the ectodermal and endodermal layers do not become separated by the intervening mesoderm and remain in close contact with each other.

The resulting double-layered plate is the cloacal membrane. When the hindgut becomes separated from the yolk sac by folds, the cloacal membrane is incorporated into the wall of the gut. The ectodermal side of the cloacal membrane is originally dorsal, but this position is inverted by the development of the tail-bud, occurring just anterior to the cloacal membrane.

The tail rudiment protrudes backward, and the hindgut above the cloacal membrane develops a diverticulum entering the tail rudiment—the postanal gut. As a result, the cloacal membrane comes to lie at the root of the tail with the ectodermal side facing downward. The part of the hindgut adjoining the cloacal membrane is somewhat dilated and becomes the rudiment of the cloaca.

The ectoderm is slightly depressed in the region of the cloacal membrane, forming the external cloaca or proctodeum. The cloacal membrane separates the cavity of the cloaca from the cavity of the proctodeum till late in embryonic development, but it is eventually ruptured and thus a free passage from the alimentary canal to the exterior is allowed.

In amphibians, reptiles, and birds, the cloaca receives the ducts carrying excretory products (the mesonephric ducts and ureters) as well as the ducts carrying eggs and sperm (the oviducts and the vasa deferentia). The cloacal opening thus serves, in these animals, for the exit of feces, urine, and sex cells.

In mammals the cloaca becomes subdivided in the course of embryonic development, so that the channel for feces is separated from the pathway serving for the conveyance of urine and sex products. This subdivision is achieved by the backward growth of a septum arising at the angle formed by the ventral surface of the gut and the allantoic stalk (“urorectal cleavage line”).

Extending backward, the septum reaches the cloacal membrane and fuses with it, thus subdividing the cloaca into a dorsal and a ventral compartment. The dorsal compartment is in continuity with the gut, and the ventral compartment receives the openings of the excretory and genital ducts, as well as the opening of the allantoic stalk.

Consequently, this compartment becomes the urogenital sinus. The inner part of the urogenital sinus with the openings of the ureters and the adjacent part of the allantoic stalk expands to form the urinary bladder. The canal leading from the bladder to the umbilicus later closes and degenerates. The portion of the urogenital sinus immediately following the bladder becomes narrow and develops as the urethra.