麻豆约拍

2000 years ago, the Roman writer Ovid wrote a long poem based on Greek myths that gained immortal fame. In 鈥淢etamorphoses鈥� (from the Greek word meaning "transformations") the poet tells stories of humans who having transgressed against the gods (usually through no fault of their own) were punished by being changed into other animals or even plants.

Written by Prof Stuart Reynolds, University of Bath.

Of course humans don鈥檛 really change into animals and plants, but the ancient Greeks and Romans knew that metamorphosis really does happen in the animal world. They were familiar with the idea that caterpillars turn into butterflies. Crucially, they had grasped the essential point which is that despite all the shape-shifting the new creature is in essence still the same individual.

Like many biologists before me, ever since I was a student I have been fascinated by metamorphosis. Lots of animals metamorphose, but we know most about insects. What can it mean for a caterpillar to turn into a butterfly, which looks so different, and yet retains its essence, the ability to reproduce and produce another caterpillar? Or is it really the winged adult butterfly that possesses the true spirit of the insect, and the wingless worm-like larva (caterpillar) is just an incompletely developed part of the adult? Surely, here must be important clues to the way that animal form is determined?

In fact, the dramatic changes of form occurring at insect metamorphosis are a consequence of the fact that insects live inside a stiff protective casing, or cuticle. As the insect develops and increases in size it outgrows this suit of armour and must replace it. Remarkably it does this from the inside, loosening the old cuticle and growing a wrinkled but larger new one inside the old. When the insect emerges it can inflate the new exoskeleton by swallowing air or water, or by squeezing body fluids from one part of the body to another. The whole process is called moulting, a term that correctly captures the idea of shedding old clothes but fails miserably to register that it first involves acquiring a pristine set of new ones.

Thinking about moulting as a change of clothes immediately suggests that it would be easy to experience metamorphosis by putting on new garments that don鈥檛 look like the old ones, like an actor changing a costume between scenes. And this is exactly what happens. While the insect retains the form of a caterpillar, each moult merely exchanges the old cuticle for a similar new one. But when the time comes for metamorphosis, caterpillar clothes are exchanged for those of the pupa or chrysalis, and then with the emergence of the adult there is a further change of garments and the creature is newly garbed in a beautiful gown of a butterfly.

The shedding of the old cuticle, a process called ecdysis, looks like a very rapid event, taking just a few minutes. But actually, this is just the culmination of moulting, a much longer process than ecdysis. This is because the new cuticle has been growing inside, hidden by the old cuticle, for much longer. Larval and pupal moults take a couple of days, but the moult that transforms the pupa to the adult takes a week or more. This is because the adult is different from the caterpillar in more ways than just skin deep. The chrysalis has an outer casing that is similar to that of the adult (it has wings for example, although as yet uninflated), but its internal organs are those of a caterpillar. Before development is completed, the butterfly needs to grow previously latent structures like reproductive organs, to develop a whole new set of nerves and muscles and integrate them with the new external skeleton, and not least to remodel its entire digestive and breathing apparatus. This takes time and is more easily accomplished if separated from the change in outward form. This is why the intermediate pupal stage intervenes.

What controls when metamorphosis takes place? We now know that moulting is triggered by a pulse of a special moulting hormone. This happens at each moult, whether it is a metamorphic moult or not. The hormone, a steroid related in chemical structure to our own sex and stress hormones, is called ecdysone, because it ultimately causes the shedding of the cuticle. But its first action is to initiate the production of a new cuticle, whose shape determines the shape of the insect that will emerge at ecdysis. The decision whether to begin metamorphosis is governed by another hormone, the juvenile hormone, produced in another endocrine gland just behind the brain. Juvenile hormone and ecdysone work together to control metamorphosis.

The juvenile hormone, exactly as its name implies, maintains the insect in an immature state as long as it is present. But when it is absent, the caterpillar transforms first to a pupa, and then to the adult stage. In a way that we don鈥檛 properly understand, the caterpillar is able to recognize when it has grown to a sufficient size, and then switches off the production of juvenile hormone.

So here is another amazing thing about insect metamorphosis: a hormone that keeps you young!

All this explains how metamorphosis occurs but it doesn鈥檛 really explain why it happens. To answer this we just have to go back to natural history. The point of metamorphosis is that it allows a greater degree of functional specialization than could otherwise be achieved. A caterpillar is literally a living eating machine, specializing on food that won鈥檛 be there forever. Plants mature and die, and the insect needs to satisfy its needs while they are still available. So day and night, it eats as fast as it can, outcompeting slower-feeding rivals. Moreover, by being quick, the period spent exposed to potential predators and parasites is minimized. One of the ways in which speed is gained is by postponing all the difficult bits of development until later; insects don鈥檛 metamorphose until they have finished eating. But when enough has been eaten, the insect can retreat to a safe place (underground or inside a silken cocoon) and take its time to transform.

The adult insect, by contrast, is specialised to reproduce. It has wings and can fly away to find a mate, or to seek out suitable food for its eggs. It is brightly colored and patterned and has special perfumes to attract mates. It has a complicated brain and sense organs to enable it to do these things. Once it has undergone metamorphosis it doesn鈥檛 grow much, and doesn鈥檛 need to feed all day like a caterpillar. In fact some adult insects don鈥檛 feed at all. In effect each individual insect embodies within its own life a division of labour, enabling each life stage to be superbly good at what it has evolved to do. Again, this was a familiar concept to the ancient Greeks. Xenophon, writing in the 4th century BC, said 鈥淥f necessity, he who pursues a very specialised task will do it best.鈥�