The epidermis and its outgrowths

The major part of the ectodermal epithelium covering the body gives rise to the epidermis of the skin. In fishes and aquatic larvae of amphibians, the many-layered epidermis is provided with unicellular mucous glands. In terrestrial vertebrates, however, the epidermis becomes keratinized; i.e., the outer layers of cells produce keratin, a protein that is hardened and is impermeable to water. During the process of keratinization, many cell components degenerate and the cells die; the layer of keratinized cells is therefore shed from time to time. In reptiles the shedding may take the form of a molt in which the animal literally crawls out of its own skin. It is less well known that frogs and toads also molt, shedding the surface keratinized layer of their skin (which is usually eaten by the animal). In birds and mammals, keratinized cells are shed in pieces that are sloughed off, rather than in extensive layers. In many vertebrates local thickenings of the keratinized layer appear in the form of claws, hooves, nails, and horns.

The epidermis is only the superficial layer of the skin, which is reinforced by the dermis, a connective tissue layer of a much greater thickness. The cells of the dermis are derived from mesoderm and neural-crest cells. In particular the pigment cells found in the dermis of fishes, amphibians, and reptiles are of neural-crest origin. The pigment in the skin of birds and mammals (and also in hairs and feathers) is also produced by neural-crest cells, but in these animals the pigment cells penetrate into the epidermis or deposit their pigment granules there.

The structure of the skin is further complicated by the development of hairs and feathers, on the one hand, and of skin glands, on the other. Hairs and feathers develop from a somewhat similar kind of rudiment. The development starts with a local thickening of the epidermal layer, beneath which a group of mesenchyme cells accumulate. In the case of hairs, the epidermal thickening proliferates downward and forms the root of the hair, from which the shaft then grows outward, emerging on the surface of the skin. In the case of feathers, the epidermal thickening bulges outward to form a hollow fingerlike protrusion with a connective tissue core. Secondarily, the shaft of the feather branches characteristically to produce barbs and barbules. In both cases, however, the final structure—shaft of the hair and shaft barbs and barbules of the feather—consists of keratinized and, thus, dead cells.

The skin of amphibians and mammals (but not of birds and reptiles) is provided with numerous skin glands, which develop as ingrowths from the epidermis. A peculiar type of skin gland is the mammary gland of placental mammals. In the first stage of development, mammary-gland rudiments resemble hair rudiments; they are thickenings of the epidermis, with condensed mesenchyme on their inner surfaces. In some mammals (rabbit, man) two continuous epidermal thickenings called mammary lines stretch along either side of the belly of the embryo. Parts of the line corresponding in number and position to the future glands enlarge while the rest of the thickening disappears. The initial thickenings proliferate inward and produce a system of ramified cords, solid at first but hollowed out later, which become the lactiferous, or milk-bearing, ducts of the gland. Further branching at the tips of the ducts gives rise to smaller ducts and to the secretory end sacs, or alveoli, of the gland.

Mesodermal derivatives

The body muscles and axial skeleton

The somites, formed in the early stages of development from the upper edges of the mesodermal mantle adjoining the notochord, are complex rudiments that subdivide and give rise to very diverse body structures. The coelomic cavity, present initially, becomes obliterated by the side-to-side flattening of the somites, so that the thinner, outer parietal layer of the somite comes in close contact with its thicker visceral layer. The visceral layer of the somite very early subdivides into two parts. The upper, dorsolateral part called the myotome remains compact, giving rise to the body muscles. The lower, medioventral part of the somite, called the sclerotome, breaks up into mesenchyme, which contributes to the axial skeleton of the embryo—that is, the vertebral column, ribs, and much of the skull. The parietal layer of the somite, at a later stage, is converted into mesenchyme that, together with components of the neural crest, gives rise to the dermis of the skin and, for this reason, is called the dermatome.

The cells of the myotome are elongated in a longitudinal direction and become differentiated as muscle fibres. The myotomes, originally situated dorsally, expand on either side, penetrating between the skin on the outside and the lateral plates of the mesoderm on the inside, until they meet midventrally; the whole body is thus enclosed in a layer of developing muscle. As the somites and myotomes are segmented, so are the muscles derived from them. Metamerism, or segmentation, a feature in the embryos of all vertebrates, remains preserved only in the adults of fishes and of terrestrial vertebrates that have elongated bodies (salamanders, snakes); it becomes largely erased in four-footed animals that depend on their limbs for locomotion.

The mesenchyme derived from the sclerotomes condenses as cartilage around the notochord and the spinal cord. It forms the cartilaginous vertebral column and ribs. In the head region it produces a part of the cartilaginous skull, mainly its posterior and ventral parts; anteriorly the somitic mesenchyme is supplemented by mesenchyme from the neural crest. Cartilaginous capsules of the olfactory organ and the ear fuse with the cartilaginous capsule surrounding the brain; to this complex are also added cartilages associated with the jaws and gill skeleton. Cartilage in the vertebral column and in the skull is replaced later in the bony fishes and in the terrestrial vertebrates by bone. At a still later stage, dermal bones are added, which, while they have no precursors in the cartilaginous skeleton, develop in the adjoining mesenchyme.

The appendages: tail and limbs

The tail in vertebrates is a prolongation of the body beyond the anus. It develops in early stages from the tail bud, immediately dorsal to the blastopore. Material for the tip of the tail is situated slightly forward from the edge of the blastopore. The elongation of the back of the body is greater than that of the belly; as a result the tip of the tail bud is carried beyond the blastopore and thus beyond the anus, which, in the developed embryo, marks the position of the blastopore. The consequence is that a section of the dorsal surface of the embryo comes to lie on the ventral surface of the tail; i.e., becomes inflected. The tail bud is formed from parts that have already been differentiated to a certain extent; prolongations of the neural tube and of the notochord are involved, and endoderm extends into the tail rudiment as the postanal gut, which, however, soon degenerates. The bud is also encased in ectodermal epidermis. In amphibians the somites of the tail are not derived from the chordamesodermal mantle but from the inflected posterior portion of the neural plate, which loses its nervous nature and becomes subdivided into segments corresponding to the somites of the trunk. In higher vertebrates the cells in the interior of the tail bud have an undifferentiated appearance and form a growth zone, at the expense of which parts of the tail (neural tube, notochord, somites) are extended backward as the tail elongates.

The paired limbs of vertebrates derive their first rudiments from the upper edge of the lateral plate mesoderm. The parietal layer becomes thickened, and cells escape from the epithelial arrangement and form a mesenchymal mass adjoining the ectodermal epithelium at the surface of the body. The ectodermal epithelium over the mass of mesenchyme likewise becomes thickened. In higher vertebrates, the accumulation of mesodermal cells and the thickening of the epidermis occur along the entire length of the trunk, from neck to anus, but in the middle of the trunk they soon disappear, and only the most anterior and the most posterior sections develop further into the rudiments of the forelimbs and hindlimbs, respectively. In fishes, the rudiments of the pectoral and pelvic fins are more extended anteroposteriorly in earlier than in final stages.

The mesodermal masses of the limb rudiments proliferate, and, covered with thickened epidermis, form on the surface of the body conical protrusions called the limb buds, which, once formed, possess all the materials necessary for limb development. Limb buds may be transplanted into various positions on the body or on the head and there develop into clearly recognizable limbs, conforming to their origin, whether a forelimb or hindlimb, a wing or a leg in birds. This specificity of the limb is carried by the mesodermal part of the rudiment, but a complex interaction between the mesodermal mesenchyme and the ectodermal epidermis is necessary for the normal development of the limb. In four-limbed vertebrates (tetrapods), the tips of the limb buds become flattened and broadened into hand or foot plates. The edge of the plate is indented, forming the rudiments of the digits. Meanwhile, local areas of the mesodermal mesenchyme in the interior of the limb rudiment condense; these are the rudiments of the various components of the limb skeleton. In fishes, small outgrowths from the myotomes enter the limb rudiment to form the muscles of the fins. In tetrapods, however, the limb muscles develop from the same mass of mesenchyme that gives rise to the skeleton. Thus the muscles of the body and the muscles of the limbs have different origins—the first develop from the myotomes (thus from the somites), and the second develop from the lateral plate mesoderm via the limb buds.

The nerves supplying the limbs grow into the limb rudiments from the spinal cord and the spinal ganglia. The nerves are guided in some way by the limb rudiments, for, if limb rudiments are displaced by transplantation to an abnormal position, the nerves still find their way and establish normal relationships to the limb muscles. Limb rudiments transplanted to sites very far from their normal positions induce local nerves to enter the limb, thereby making it motile.

Excretory organs

The kidneys of vertebrates consist of a mass of tubules that develop from the stalks of somites called nephrotomes. In some primitive vertebrates such as cyclostomes, the nephrotome in each segment gives rise to only one tubule, but, in the great majority of vertebrates, mesenchyme from adjacent nephrotomes fuses into a common mass that differentiates into a number of nephric tubules irrespective of the original segmentation of the mesoderm. Under primitive conditions each tubule opens by a funnel (the nephrostome) into the coelomic cavity; the opposite ends of the tubules fuse to form the collecting ducts of the kidney. A collection of capillaries (the glomerulus) becomes associated with the nephric tubule, forming its filtration apparatus. The glomerulus may be situated in the coelomic cavity opposite the nephrostome or, in all the more advanced animals, intercalated into the nephric tubule, forming with the latter a renal corpuscle of the kidney. In adults of all vertebrates above the amphibians, the nephrostomes disappear (or are never formed), so that the tubule begins with the renal corpuscle. Parts of the kidney in vertebrates can be distinguished as the pronephros (most anteriorly, at the forelimb level), the mesonephros (in the midtrunk region), and the metanephros (in the pelvic region). The three sections of the kidney develop at different stages, starting with the pronephros and ending with the metanephros. In their morphology and mode of development, the anterior parts show more primitive conditions than the posterior ones. The pronephros, developing early in embryo formation, is the functional kidney of fish and amphibian larvae. Its collecting duct opens into the hindmost part of the intestine, called the cloaca, and later also serves as the collecting duct of the mesonephros. In reptiles, birds, and mammals, the pronephros is nonfunctional, although even in these animals its duct persists as the mesonephric duct. The mesonephros develops later and replaces the pronephros as the functional kidney of adult fishes and amphibians and of the embryos of reptiles, birds, and mammals. The tubules of the mesonephros link up with the duct derived from the pronephros. The pronephric duct in fact stimulates the development of mesonephric tubules, and, in its absence, the mesonephros does not develop at all.

The metanephros is found only in reptiles, birds, and mammals. It replaces the mesonephros of the early embryonic stages and continues as the functional kidney in the postembryonic and adult life of these animals. The metanephros develops from mesenchyme derived from the nephrotomes of the posterior part of the trunk and lying dorsal to the mesonephric duct. The actual differentiation is initiated by a dorsal outgrowth of the mesonephric duct, called the ureteric bud. The ureteric bud grows in the direction of the mesenchyme and becomes the ureter. Having penetrated the mass of mesenchyme, it starts to branch, producing the collecting tubules of the kidney; the mesenchyme, meanwhile, in response to the influence of the duct and its branches, aggregates to form the excretory tubules of the kidney. The influence of the ureter is indispensable for the development of the metanephric excretory tubules, for, if the ureter fails to develop or, in its outgrowth, stops short of reaching the kidney-producing mesenchyme, no kidney develops.

Circulatory organs

The rudiment of the heart in vertebrates develops from the ventral edges of the mesodermal mantle in the anterior part of the body, immediately adjoining the pharyngeal region. A group of mesodermal cells breaks away from the ventral edge of the lateral plate, takes a position just underneath the pharyngeal endoderm, and becomes arranged in the form of a thin-walled tube, which will become the endocardium, or lining of the heart. In vertebrates with complete cleavage, the endocardial tube is single and medial from its start. In higher vertebrates with meroblastic cleavage—reptiles, birds, and mammals—the embryo in early stages of development is flattened out on the surface of the yolk sac; therefore, what are morphologically the ventral edges of the mesodermal mantle lie far apart on the perimeter of the blastodisc. As a result of this arrangement, two endocardial tubes are formed, one on either side of the embryo. Subsequently, when the embryo becomes separated from the yolk sac, the two endocardial tubes meet in the midline ventral to the pharynx and fuse, producing a single heart rudiment. After the formation of the endocardium, or the lining of the heart, the coelomic cavity in the lateral plate mesoderm adjoining the heart rudiment expands slightly and envelops the endocardial tube or tubes. The heart muscle layer, or myocardium, develops from the visceral (splanchnic) layer of the lateral plate that is in contact with the endocardial tube; the parietal (somatic) layer of the lateral plate forms the pericardium, or covering of the heart. The portion of the coelom surrounding the heart becomes separated from the rest of the body cavity and develops into the pericardial cavity.

The endocardial tube branches anteriorly into two tubes, the ventral aortas; a similar branching of the endocardial tube posteriorly forms the two vitelline veins, which carry blood from the midgut endoderm or from the yolk sac (when present) to the heart.

In its earliest development, the heart rudiment shows a degree of dependence on the adjoining endoderm. The whole of the endoderm can be removed in newt embryos in the neural-tube stage. In such endodermless embryos, the heart fails to develop, even though the mesoderm destined to form the heart rudiment is left intact.

The heart is initially a straight tube stretching in an anteroposterior direction. Rather early in development, however, it becomes twisted in a characteristic way and subdivided into four main parts: the most posterior, the sinus venosus; the atrium, which comes to lie at the anteriorly directed bend of the tube; the ventricle, occupying the apex of the posteroventrally directed inflexion; and, most anteriorly, the conus arteriosus. In the course of development in the more advanced vertebrates, the atrium and ventricle become partially or completely subdivided into right and left halves. In amphibians, only the atrium is separated into two halves, by a partition starting from the posterior end. In reptiles, a partition separates the atria and part of the ventricle. In birds and mammals, the subdivision of the heart is complete, with two atria and two ventricles.

The complete subdivision of the heart is important for separating the pulmonary, or lung, blood supply from the general body circulation. But, if this separation developed early in the embryo, it would create difficulties, since the lungs of the embryo are not functional; the enrichment of the blood with oxygen occurs instead in the placenta. The partition between the atria in mammalian embryos remains incomplete, so that blood returning from the body and from the placenta enters into the right half of the heart but is shunted (through the interatrial foramen) into the left half of the heart and thence again into general circulation. At birth, however, the interatrial foramen is closed by a membraneous flap, and oxygen-depleted blood from the body enters the right atrium, is channelled into the right ventricle, and thence to the lungs for oxygenating.

In an adult vertebrate, blood vessels extend to all parts of the body. It would seem that channels for the supply of blood are provided in proportion to the local demand of the tissues; progressively developing organs or parts with particularly intensified function always receive an increased blood supply. The rudiments of blood vessels are always aggregations of mesenchyme cells. In any blood vessel the endothelial tube is formed first, and the muscular and elastic layers are added later.

The main blood channels in vertebrates develop in certain favoured situations; namely (1) between the endoderm and lateral plate mesoderm; (2) around the kidneys, especially the pronephros and mesonephros; and (3) in connection with the heart, which is a special case of the first category.

From the paired forward extensions from the heart, the ventral aortas, loops develop between the pharyngeal clefts. These are the aortic arches, which served originally to supply blood to the gills in aquatic vertebrates. The arches are laid down in all vertebrates, six or more being found in cyclostomes and fishes; six are present in the embryos of tetrapods, but the first two are degenerate. The arches of the third pair develop as the carotid arteries, supplying blood to the head. Those of the fourth pair (and, exceptionally, in urodeles also the fifth) join dorsally to form the dorsal aorta, providing blood to most of the body. These are the systemic arches. The arches of the sixth pair are the pulmonary arches; in embryos they carry blood to the dorsal aorta, as well as to the lungs, but in fully developed amniotes (reptiles, birds, and mammals), they carry blood only to the lungs.

The paired posterior extensions of the heart of the early embryo are the vitelline veins, whose branches spread out between the lateral plate mesoderm and the endoderm, especially the endoderm of the yolk sac, when present. On their way to the heart, the vitelline veins pass through the liver and break up into a system of small channels—the hepatic sinusoids. Parts of the vitelline veins lying posterior to the liver become the hepatic portal veins, which carry blood from the intestine to the liver; the parts of the vitelline veins anterior to the liver become the hepatic veins, which carry blood from the liver to the sinus venosus in lower vertebrates (anamniotes), but become the anterior section of the postcaval vein in amniotes.

Whereas the vitelline veins and, later, the hepatic portal vein carry blood from the endodermal parts of the embryo and from the yolk sac to the heart, the blood from the mesodermal and ectodermal parts is returned to the heart through a system of cardinal veins. These latter veins start their development in the form of an irregular sinus around the pronephros, connected by the common cardinal veins (ducts of Cuvier), on either side, to the sinus venosus. Extensions anteriorly and posteriorly give rise to the precardinal and postcardinal veins, respectively. The postcaval vein, present in terrestrial vertebrates, is a late acquisition, both in evolution and in embryogenesis; it is a result of the intercommunication of several venous channels, including the anterior portion of the vitelline veins.

The first blood cells in vertebrate embryos form in association with the intestinal endoderm on the yolk sac. Groups of mesoderm cells derived from the splanchnic layer of the lateral plate (extra-embryonically in cases in which a yolk sac is present) become so-called blood islands, which are particularly conspicuous on the yolk sac of bird embryos (in the area vasculosa). In bird’s eggs, the internal cells of the blood island start producing hemoglobin (gas-carrying component of blood) and become the first red blood cells (erythrocytes) as early as the second day of incubation. The outer cells of the blood islands develop into an endothelial layer and form a network of blood vessels covering part of the surface of the yolk sac. The network acquires a connection to the vitelline veins and vitelline arteries (the latter being branches of the dorsal aorta); thus the blood corpuscles formed in the blood islands can enter the general blood circulation.

At later stages of embryogenesis, blood-cell formation shifts from the blood islands to the liver and, still later, to the bone marrow.

The lymphatic system, in a manner similar to the blood vessels, develops by the local aggregation of connective tissue to form lymphatic vessels.

Reproductive organs

In considering the development of reproductive organs, distinctions must be made between: (1) the origin of sex cells (gametes), (2) the origin and differentiation of the sex glands, or gonads (ovaries and testes), and (3) the origin and development of the supporting parts of the reproductive system (e.g., genital ducts, copulatory organs).

The germ (germinal) cells, which eventually give rise to the gametes, are often segregated from the somatic, or body, cells at a very early stage—during cleavage and before the subdivision of the embryo into ectoderm, mesoderm, and endoderm. In the invertebrate nematodes, the very first of these primordial germ cells is identifiable after as few as five divisions of the egg cell. The germ cell retains the large chromosomes present in the fertilized egg; in the somatic cells the chromosomes become fragmented. Subsequently, the single germ cell gives rise, by mitotic divisions, to all the gametes in the gonad.

In vertebrates, primordial germ cells arise outside the gonads, but they cannot be distinguished in early cleavage stages. In amphibians, cytoplasm at the vegetal pole, rich in ribonucleic acids, becomes incorporated into a number of cells, which, during cleavage and gastrulation, lie among the yolky endoderm cells. Later they migrate into the mesodermal layer and become incorporated into the rudiments of the gonads. In higher vertebrates, primordial germ cells can be recognized in the extra-embryonic endoderm of the yolk sac. In mammals, these cells subsequently migrate into the mesoderm and are located in the gonad rudiments. The mouse embryo, for example, originally has fewer than 100 primary germ cells; during their migration, however, their numbers increase as a result of repeated divisions, to 5,000 or more in the gonads.

Although the primordial germ cells either may appear before the separation of germinal layers or be found originally in the endoderm, the gonads are invariably of mesodermal origin. In vertebrates, the first trace of gonad development is a thickening of the coelomic lining on either side of the dorsal mesentery and medial to the kidney rudiments. The thickening, elongated anteroposteriorly, is known as the germinal ridge. The ridge protrudes into the coelomic cavity, and the fold of thickened epithelium becomes filled with mesenchyme. At this stage the primordial germ cells invade the rudiments of the gonads and become associated with the somatic cells of the germinal ridge. In the functionally differentiated gonads, only the actual gametes and their predecessors (spermatogonia and oogonia) are derived from the primary germ cells; the supporting cells are somatic cells of local mesodermal origin. In the ovaries, the follicle cells surrounding and nourishing the young egg cells (oocytes) are of somatic origin, as are also the connective tissue and blood vessels of the gonad. In the testes, supporting elements called Sertoli cells are somatic cells, as are the interstitial cells, which are scattered between the sperm-carrying tubules of the testes and believed to be the source of male hormones.

In the early stages of their development—even while the gonad rudiment is being invaded by primordial germ cells—the female and male gonads are in an indifferent stage. Only later does tissue differentiation of the gonads begin and male or female gonadal development proceed.

The genital ducts, by which the eggs and sperm are carried away from the gonads, are, in vertebrates, linked with the excretory system. In the male, the seminiferous tubules connect with the nephric tubules of the mesonephros, and the sperm are carried to the exterior by way of the mesonephric duct. In males of lower vertebrates, the mesonephric duct thus serves as a channel both for urine and for sex cells. In amniotes the development of the metanephros as the urine excreting organ has freed the mesonephric duct to carry products associated only with reproduction. In the female, a separate duct, the paramesonephric duct (Müllerian duct), develops beside the mesonephric duct. At its anterior end it utilizes the funnels of the pronephric tubules as its entrance (ostium). The paramesonephric duct develops initially in both female and male embryos. The ducts remain in an indifferent stage longer than the gonads. Eventually the sex hormones produced by the differentiating gonads cause a corresponding differentiation of the ducts. The mesonephric ducts, which become reduced in female embryos, remain in male embryos as ducts for conveying sperm (ductus deferens). The paramesonephric ducts, on the other hand, degenerate in male embryos but become the oviducts in female embryos. In mammals, the terminal portions of the paired oviducts differentiate as two uteri, which, in primates and man, fuse to form a single uterus.

In all terrestrial vertebrates except the placental mammals, the genital ducts, as well as the ducts of excretory organs, open into the cloaca. In mammals, however, the cloaca becomes subdivided into a dorsal part, which conveys the feces, and a ventral part, which receives excretory and genital products. In male mammals the excretory and genital ducts remain connected, having the urethra as their common outlet; in females the urethra serves only for the passage of urine and the uterus opens separately by means of the vagina. In nearly all vertebrates, the male nephric duct is utilized in some degree for the conduction of sperm.

Copulatory organs have developed independently in several groups of vertebrates having internal fertilization. The penis in mammals develops from an outgrowth called the genital tubercle, located at the anterior edge of the urinogenital orifice. The tubercle is laid down in a similar way in embryos of both sexes, and the region of the urinogenital orifice remains in an indifferent state even longer than do the genital ducts. In a comparatively late stage of embryonic life the genital tubercle of male embryos encloses the urethral canal and becomes the penis; in female embryos it remains small and becomes the clitoris.

Endodermal derivatives

The alimentary canal

The alimentary canal is the chief organ developing from endoderm. The way it forms depends on the type of egg cleavage. In eggs with holoblastic (complete) cleavage, after gastrulation the invaginated mass of endoderm lines the archenteron, the cavity of which becomes the alimentary canal, or gut. In eggs with meroblastic (partial) cleavage—and also in mammals (despite their complete cleavage)—the endoderm is produced in the form of a sheet lying flat over the yolk-sac cavity. Subsequently, folds of endoderm and splanchnic mesoderm appear—first anteriorly, then laterally, and lastly posteriorly—and sink, converging ventrally under the embryo and cutting off the future gut cavity from the cavity of the yolk sac. The most anterior and posterior portions of the gut separate, but the middle part remains in open communication with the yolk sac throughout embryonic life, eventually becoming reduced to the yolk stalk, which passes through the umbilical cord.

The alimentary canal of vertebrates becomes differentiated into the oral cavity, pharynx, esophagus, stomach, and intestine. Whether derived from an archenteron or formed by folding of the endodermal sheet, the canal initially does not possess an opening at its anterior end. This is also the case in some lower chordates and echinoderms, which are grouped together with vertebrates as the Deuterostomia, or animals with secondary mouths.

In vertebrates, a mouth forms by a rupture at the anterior end, where the endoderm is in contact with ectoderm. The ectoderm of the future mouth region becomes depressed, forming a mouth invagination, or stomodaeum. The ectodermal and endodermal layers separating the cavity of the stomodaeum from the gut fuse to form the oropharyngeal membrane, which thins and ruptures, providing free passage from the exterior to the gut. Because of its mode of origin, the oral cavity is in part lined by ectoderm and in part by endoderm, the two parts becoming indistinguishable. Before the oropharyngeal membrane ruptures, however, a small pocket forms on the dorsal side of the stomodaeal invagination. This, the rudiment of the anterior lobe of the hypophysis, becomes apposed to the ventral surface of the diencephalon and loses its connection with the mouth cavity.

The anal opening in some exceptional cases (urodele amphibians) is derived directly from the blastopore, which persists as a narrow canal after completion of gastrulation. In other vertebrates, however, the anus develops either near the location of the former blastopore or in a corresponding region at the posterior end of the embryo, where the last remnants of mesoderm migrated to the interior. It is thus claimed that the anus in vertebrates is derived, directly or indirectly, from the blastopore. The mode of formation of the opening is somewhat similar to that of the mouth. A slight invagination of the ectoderm occurs, and a cloacal membrane forms, separating the ectodermal invagination from the gut cavity. The membrane ruptures later to provide the anus.

The pharynx and its outgrowths

The anterior portion of the endodermal gut, lying immediately posterior to the mouth cavity, expands laterally as the pharynx. The lateral pockets of the pharyngeal cavity, called the pharyngeal pouches, perforate the mesodermal layer, reach the ectoderm, and break through to form pharyngeal, or gill, clefts. In fishes and larvae of amphibians, these clefts develop gills and become respiratory organs. Pharyngeal pouches develop in the early embryos of all vertebrates, including the air-breathing terrestrial reptiles, birds, and mammals. The number of pouches has been reduced in the course of evolution from six or more to four in tetrapods, and the posterior pouches may not actually break through.

The consistent development of pharyngeal pouches and clefts indicates their importance in vertebrate development. Many parts of the vertebrate body are derived from, or dependent on, the pharyngeal pouches; for example, the aortic arches—the most important blood vessels of a vertebrate—develop between successive pharyngeal pouches. Skeletal visceral arches also occur between consecutive pharyngeal pouches (they do not develop if the pharyngeal pouches are prevented from developing). In adult terrestrial vertebrates, parts of the visceral arches are transformed into the hyoid apparatus, supporting the tongue, the auditory ossicles, and parts of the larynx and trachea. Furthermore, some of the material of the pharyngeal pouches is utilized for the formation of the parathyroid glands and the thymus; the former are indispensable glands of internal secretion, and the latter are a source, in mammals, of cells that produce antibodies. The pharynx also produces the rudiment of the thyroid gland as a ventral outgrowth.

The liver, pancreas, and lungs

Three additional important organs develop from the endoderm: the liver, the pancreas, and the lungs. The liver develops as a ventral outgrowth of the endodermal gut just posterior to the section that eventually will become the stomach. Initially, the liver takes the form of a tubular gland, but it soon acquires a close relationship to the blood sinuses and capillaries, forming lobules around blood vessels rather than around glandular ducts. The pancreas develops from three independent rudiments: two ventral ones, formed just posterior to the liver rudiment, and a dorsal one. The ventral and the dorsal rudiments fuse in most vertebrates to form one organ with a complicated system of ducts opening into the duodenum, a portion of the small intestine. The lungs develop from a ventral hollow outgrowth of the gut, which is located just posterior to the pharyngeal region; the outgrowth branches into a right and left trunk that grow posteriorly beside the esophagus and then expand into hollow sacs, in lower terrestrial vertebrates, or into a system of tubes, in birds and mammals.

The endodermal parts of the alimentary system are, along their entire length, encased by the splanchnic mesoderm of the lateral plates. The coelomic cavities of the right and left sides fuse ventral to the gut but remain separated dorsally by their respective walls, which form the dorsal mesentery—a double membrane by which the gut is suspended from the dorsal side of the body cavity and through which blood vessels and nerves reach the gut. The layer of splanchnic mesoderm next to the endoderm produces the connective tissue and muscular layers of the gut. During development of the glands of the alimentary canal (e.g., pancreas, salivary glands), the mesoderm forms a connective tissue capsule around the branching tubules of the gland. The development of the tubules is dependent on this mesodermal capsule and cannot proceed without it.

Postembryonic development

After partially developing within the egg membranes or within the maternal body, the newly formed individual emerges. The new animal is then born (ejected from the mother’s body) or hatched from the egg. The condition of the new organism at the time of birth or hatching differs in various groups of animals, and even among animals within a particular group. In sea urchins, for example, the embryo emerges soon after fertilization, in the blastula stage. Covered with cilia, the sea-urchin blastula swims in the water and proceeds with gastrulation. Frog embryos emerge from the egg membranes when the main organs have already begun to develop, but functional differentiation of the tissues is unfinished; for instance, the components of the eyes and ears are far from complete, the mouth is not yet open, and the gut is filled with yolk-laden cells. Certain birds (called precocial) emerge from the egg covered with downy feathers and can run about soon after hatching, whereas others (altricial) hatch naked, with only rudiments of feathers, and are quite unable to move around. Among mammals there is a great range in the degree of development at birth. In marsupials, such as opossums and kangaroos, the young are born incompletely developed and very small; the young are then kept for a long time in the pouch of the mother, all the while firmly attached to the teats and suckling. Many small mammals are helpless at birth. Mice are born naked and blind; puppies and kittens are born covered with fur but with unopened eyes. Newborn human babies have their eyes open but cannot move themselves about for several months. Hoofed mammals, on the other hand, bear young that can stand up and run after their mothers within a few hours of birth.

In birds the hard shell is broken by the hatchling’s beak, which is provided with a sharp tubercle on its top. A similar “egg tooth” appears on the tip of the snout of hatchling reptiles. Many arthropods have a preformed line of fragility that allows part of the eggshell to be burst open like a lid, allowing the young to emerge. Birth in mammals is effected through the contraction of smooth muscles of the uterus.

The larval phase and metamorphosis

The organism emerging from the egg or from the maternal body, apart from being incompletely developed, may have an organization more or less different from that of an adult. In some cases the difference is so great that, without knowing the origin of the eggs or without following the young through their full course of development, it would be impossible to know that the young and the adult are of the same animal species. Such young, called larvae, transform into the adult form by a process of metamorphosis. The term larva also applies to young that resemble the adult form but differ from it in some substantial respect, as in possessing organs not present in the adult or in lacking an important structure (apart from sex glands and associated parts, which tend to develop later in life in most animals). Larvae in different animals have special names given to them, such as the tadpole of frogs, the caterpillar of butterflies, and the fry of fishes.

The larval stage

The development of the embryo into a larva rather than directly into an organism similar to the adult has various advantages. At the time of emergence from the egg, the new individual is relatively small, and the organization that enables the adult to lead a particular mode of life may not be suitable for a miniature copy of the adult. The larva may have to procure food for itself and, being small, may not be able to feed in the same way as the adult. It also may not be able to use effectively the same defense mechanisms the adult possesses. The larval stage enables an animal to avoid such hazards; it provides a mode of life and corresponding organization better suited to the smaller size of the newly emerged organism. Another advantage is that the larva may be able to exploit an entirely different environment because its organization is very different from that of the adults. A terrestrial adult may have aquatic larvae, a flying adult may have burrowing larvae, and a parasitic adult may have a free-living larva. A third advantage of a larval stage emerges in