Metamorphosis

Unlike mammals, most animals become adults by first going through a distinctly different immature, or larval, stage of development. Larvae look nothing like the adults they will form. They are specialized primarily for growth and feeding and are unable to reproduce. At a certain time in their growth, often in response to signals from hormones or the environment, the larva undergoes a second spurt of development called metamorphosis.

The word “metamorphosis” comes from the Greek word for transformation and is defined as a major change in body form that occurs after embryonic development is completed. Metamorphosis is very widespread in the animal kingdom, but it has been studied most thoroughly in three different groups of organisms: the arthropods (crabs, lobsters, and insects), the amphibians (frogs and salamanders), and the echinoderms (sea urchins and starfish).

Metamorphosis affects the ways animals eat, breathe, and move. It can also change the nature of the environment in which they live. In echinoderms, the larval stage is microscopic and free swimming, while the adults are large and move very little, if at all. The changes in body form thus coincide with significantly different ways of feeding and moving.

Amphibian Metamorphosis

In amphibians, metamorphosis prepares the organism for its transition from living in water to living on land. Internally, the digestive system changes to accommodate the new diet as the animal switches from consuming plants to animals. Sense organs like the eyes and ears also change to adapt to functioning predominantly in air. Finally, many of the chemical reactions which occur in the individual cells of the frog also change at this time.

Metamorphosis in amphibians is controlled by a pair of hormones. Prolactin, a protein secreted by the anterior pituitary gland, controls the rate of growth of the tadpole and suppresses metamorphosis. Thyroxine is a modified amino acid made in the thyroid gland of the tadpole and causes metamorphosis to begin. After the tadpole has grown to a certain minimal size, the thyroid gland is stimulated by environmental conditions to produce large quantities of thyroxine, which reverses the suppression exerted by prolactin and begins metamorphosis. The hormones pass through the tadpole’s circulation and instruct different tissues to activate and deactivate different sets of genes that cause some tissues to degenerate, others to change, and others to grow.

These same hormones, prolactin and thyroxine, are produced by other vertebrates; nature often uses the same molecules to produce very different results in different animals. In humans, thyroxine regulates the rate of metabolism, while prolactin is crucial for milk production in nursing women. In fish, however, prolactin is crucial for keeping the cell’s content of salt in balance.

Insect Metamorphosis

The hormonal control of metamorphosis in one group of animals, the insects, has yielded basic information about how genes and hormones interact to guide development in all animals. This process is understood in greater detail in insects than in any other group of animals.

Insects, like all arthropods, have a rigid exoskeleton, called a cuticle, that supports their body mass and allows the attachment of muscles for movement. Because it is external and fixed in size, however, the cuticle must be shed periodically for growth to occur. The process of insects shedding their cuticle and producing a new, larger one is called molting, and the number of molts normally occurring is regulated by the insect’s genes. Many insects have developed complex behaviors to ensure that they molt in a secluded location and avoid predation. Without their hard, external covering, they are relatively defenseless.

About 10 percent of all insect species, such as the grasshoppers and true bugs, go through a process of incomplete metamorphosis. Here, the egg hatches into a juvenile form called a nymph that resembles the adult but is much smaller and is not capable of reproduction. At each molt, the nymph sheds its cuticle and grows before the newly produced cuticle hardens. When the signal for metamorphosis arrives, the molt produces an adult, often with wings, but, more important, fully capable of reproduction. Male and female adults can then mate and lay a new generation of eggs.

Complete metamorphosis, on the other hand, is a very different process that is undergone by 90 percent of all species of insects, including the ants, bees, flies, butterflies, and moths. Here, the larval form looks nothing like the adult. For example, the larval form of a butterfly is a caterpillar, and the larval form of a fly is a wormlike maggot. Each larva undergoes a series of molts to be able to grow. The larva of the cecropia moth increases in mass by five thousand times during its larval development. When the trigger for metamorphosis occurs, the insect undergoes a radical change. The larva stops feeding and moving, anchors itself to a twig, leaf, or rock, and either spins a cocoon or encloses itself in its own hardened cuticle.

Silkworm Metamorphosis

The silkworm, Bombyx mori, undergoes complete metamorphosis, and its development begins when the egg hatches and includes five distinct larval stages. Each stage is larger than the one preceding as the larva eats, voraciously consuming several times its own body weight in food each day. At the end of the fifth larval stage, the molting event that follows is very different from the previous larval molts as the caterpillar spins a cocoon made of silk (which is the commercially valuable product of this organism) and becomes a pupa. The next molt occurs within the pupal case when metamorphosis begins. When the adult has formed, the cocoon breaks open and the adult emerges to begin reproduction.

Metamorphosis involves the complete replacement of one body form with another. Inside the pupal case, the larval tissues break down and their molecules are reutilized in the construction of the cells and tissues of a very different looking animal, the adult. Certain groups of cells, called imaginal disks, along with the larval brain, are generally the only tissues that are not broken down in this process. Opening a cocoon at this time shows that it is filled with a white, milky sap and little else as the caterpillar has been completely broken down.

The imaginal disks, round, flat sheets of cells, begin to evert or “telescope” and form the external structures characteristic of the adult cuticle. There is an imaginal disk for each eye, for each antenna, for the two or four wings, and for each of the six legs. These structures attach and the adult insect is constructed. In the well-studied fruit fly, Drosophila, this process takes about a week, while it can take months for other insects.

Hormonal Regulation of Metamorphosis

In insects, three very different hormones combine to regulate the timing of both molting and metamorphosis. Each of these three hormones is produced in a different tissue, and each has a different chemical structure and mode of function. The signal to molt originates in a small group of cells within the caterpillar’s brain in response to neural or environmental signals. The hormone produced there, prothoracicotropic hormone (PTTH), is a small protein that passes through the insect’s hemolymph (blood) to all parts of the body. As is true of all hormones, only certain target tissues are genetically programmed to respond to the production of this hormone. In this case, the prothoracic gland responds by producing a second hormone called ecdysone, the molting hormone. Ecdysone is a steroid, a chemical derivative of the cholesterol that the insect requires in its diet. Ecdysone is not actually the molting hormone itself but must first undergo some minor chemical changes before it becomes active. More important, ecdysone and its derivatives are the molting hormone not only for all insects, but for all arthropods and many other animals. This chemical signal thus evolved before divergence of these organisms from a common ancestor.

Different tissues respond differently to ecdysone, but the hormone’s major effect is to trigger molting by causing the hardening of the cuticle and the separation of the living cells beneath the cuticle from it. The cuticle then dries and cracks, and the larva can then emerge from its old skin and grow. If PTTH production stops, the amount of ecdysone released from the prothoracic gland also falls. This happens normally in the period between molts but can also occur during a molt. In cecropia moths, the level of PTTH drops during the pupal stage and the subsequent drop in ecdysone production causes diapause, a programmed pause in development. The pupa will remain in diapause until an environmental signal, consisting of a minimum of two weeks in the cold followed by a normal spring warming, triggers the resumption of PTTH secretion and the completion of metamorphosis.

Ecdysone acts specifically on certain groups of insect genes and not others. Many genes required for larval functions are turned off in response to ecdysone, while those genes required for molting and metamorphosis are turned on. This effect can be seen when imaginal disks are placed in a culture dish along with physiological levels of ecdysone. The disks stop growing and begin metamorphosis. Such development can even produce normal-looking legs floating free in a culture dish. The changes in shape of the disk cells can be directly attributed to the function of genes turned on by ecdysone.

The hormone ecdysone, therefore, not only causes metamorphosis, but also triggers certain simple molts. The third hormone involved in the control of metamorphosis is responsible for this choice, the choice to molt and grow or to undergo metamorphosis to the adult form. This compound is called juvenile hormone (JH). JH is produced in a gland called the corpora allata, and the hormone has yet a third chemical structure, a derivative of a class of molecules called terpenes. Unlike ecdysone, however, the JH of each species has a different chemical structure.

When a molt is triggered by the production of ecdysone, the type of molt that occurs will be determined by the level of JH present. During larval development, the amount of JH in the hemolymph is high, and the tissues respond to ecdysone by undergoing a molt to become a larger larva. Later in development, the corpora allata stops producing JH, and any new molt triggered by ecdysone causes the organism to proceed to the pupal stage and begin metamorphosis. The interaction of ecdysone and JH thus governs which type of molt will occur.

Although these hormones are crucial for controlling molting and metamorphosis, they play other roles as well. For example, adult female insects produce large quantities of ecdysone and adult males do not because ecdysone is important to egg production.

Laboratory Studies of Metamorphosis

Various parts of the elaborate interplay of the three hormones that regulate metamorphosis in insects were discovered in a number of laboratories. The role of ecdysone was discovered first by Carroll Williams and Vincent Wigglesworth, who found that the prothoracic gland of the larva was responsible for producing a substance that triggered metamorphosis. They tied a fine string around the middle of a cecropia larva and observed that only the front half underwent metamorphosis. The signal was thus produced somewhere in the front half and could not reach the rear of the insect. The prothoracic glands were later discovered to be the source of the molting signal when glands transplanted to the rear half of a ligated larva caused metamorphosis to occur there as well.

Ecdysone was painstakingly purified and chemically identified by Peter Karlson’s group in Germany. In a monumental effort, they extracted twenty-five milligrams of pure ecdysone from a ton of silkworms. Much of the difficulty encountered in this isolation stemmed from the lack of an easy method for identifying the presence of ecdysone in the extract they were producing.

A tedious and relatively insensitive bioassay was used. In this assay, the extract to be tested during the isolation was dissolved in an organic solvent and painted on the cuticle of an insect. If the extract contained ecdysone, the larva would begin to molt. Although time-consuming and not very reproducible, the bioassay allowed the purification of ecdysone from insects.

The role of the corpora allata and JH was found by a similar set of experiments. Wigglesworth found that if he decapitated a fourth-stage Rhodnius nymph and sealed the body with wax to that of a decapitated fifth-stage nymph, the insects could survive for a long period of time. This technique is called parabiosis. The mature nymph never underwent metamorphosis but rather molted in response to its own ecdysone or to ecdysone painted on its cuticle to form a larger nymph. Once again, tissue transplantation experiments showed that the hormone coming from the immature nymph that prevented metamorphosis was produced by the corpora allata. Removing the corpora allata from a larva or nymph caused either death or premature metamorphosis to the adult stage.

The role played by PTTH was also elucidated by a similar set of surgical experiments. Removing the brain of a larva prevented the production of ecdysone from the prothoracic gland so long as the removal occurred before the brain released the PTTH. After the PTTH signal was released, removing the brain had no effect on the subsequent production of ecdysone for that molt.

Today, the presence and amount of the three hormones are measured by easy, sensitive, and highly reproducible immunological techniques. In these procedures, antibodies, proteins having the chemical ability to bind tightly to a specific insect hormone, are produced. If an extract contains one of these hormones, adding its specific antibody will cause the hormone to bind to the antibody, and the amount of bound antibody can be accurately measured in a number of different ways.

These immunological procedures have allowed researchers to monitor the changing levels of the three hormones during the development of any insect and to correlate these changes with the progress of metamorphosis. Coupled with new information about the ability of hormones to turn genes on and off directly, these procedures have advanced the understanding of the mechanisms of control of metamorphosis at the molecular level.

Principal Terms

Corpora Allata: A gland in insects that synthesizes and secretes juvenile hormone (JH)

Ecdysone: A hormone that triggers both molting and metamorphosis in insects as well as in many other species of animals

Imaginal Disk: Flat sheets of cells within an insect larva; these cells will change shape during metamorphosis and form the external structures of the adult

Juvenile Hormone (JH): A species-specific hormone which controls whether a molt will produce a larger larva or initiate metamorphosis

Larva: The reproductively immature feeding stage in the development of many species of animals, including those insects which undergo complete metamorphosis

Nymph: The sexually immature feeding stage in the development of those insects which undergo incomplete metamorphosis

Prothoracic Gland: The gland where ecdysone is made in insects

Prothoracicotropic Hormone (PTTH): A hormone made in the brain of insects which stimulates the prothoracic gland to make ecdysone

Pupa: The stage of insect development during which metamorphosis occurs

Bibliography

Basu, Lex. "5 Animals That Go Through Metamorphosis & How They Do It." A-Z Animals, 21 June 2023, a-z-animals.com/blog/5-animals-that-go-through-metamorphosis-how-they-do-it. Accessed 4 July 2023.

Danks, H. V., ed. Insect Life-Cycle Polymorphism: Theory, Evolution, and Ecological Consequences for Seasonality and Diapause Control. Kluwer, 1994.

DePomerai, David. From Gene to Animal. 2nd ed. Cambridge University Press, 1990.

Gilbert, Lawrence I., and Earl Frieden, eds. Metamorphosis: A Problem in Developmental Biology. 2nd ed. Plenum, 1981.

Gilbert, Scott F. Evolutionary Developmental Biology. Elsevier, 2021.

Koolman, Jan, ed. Ecdysone: From Chemistry to Mode of Action. G. Thieme Verlag, 1989.

Raven, Peter H., and George B. Johnson. Biology. 13th ed. Times Mirror/Mosby, 2022.