How Does a Caterpillar Become a Butterfly? What Happens Inside the Chrysalis

A butterfly's life has four stages: egg, larva, pupa and adult. The larva, the caterpillar, exists to eat. It has a chewing mouth, a simple gut that runs the length of its body, stubby legs, eyes that can barely tell light from dark, and no wings, and it can multiply its weight a thousand times in a few weeks, shedding its skin four or five times as it outgrows it. The adult exists to reproduce and disperse. It has wings, long legs, compound eyes, antennae, a coiled tube for drinking nectar and no ability to chew at all. The two forms share almost no organs and eat entirely different food, so they do not compete with each other, which is thought to be the main reason the arrangement evolved.

When the last caterpillar skin is shed, what emerges is the pupa, and in butterflies it hardens into the chrysalis. Inside, the caterpillar's cells begin to die in an orderly, programmed way, and enzymes break the muscles, gut and glands down into their components. The raw material is used to grow the imaginal discs: small flat pockets of cells, a few thousand each, that have been present since the embryo and that each hold the pattern for one adult part, a wing, a leg, an eye, an antenna. Each disc unfolds and grows into its structure, drawing on the soup around it, and over a week or two the adult assembles itself. The sequence:

• •The caterpillar stops eating, empties its gut, spins a silk pad and hangs from it
• •It sheds its final skin and the pupal case hardens beneath
• •Larval tissues are broken down by programmed cell death and digestive enzymes
• •The imaginal discs grow into wings, legs, eyes, antennae and mouthparts
• •The adult's muscles and nervous system are rebuilt, partly from surviving larval cells
• •The adult pumps fluid into its wing veins, breaks out of the case, and hangs while the wings dry and harden

Two hormones run the timetable. Ecdysone, released from a gland in the thorax, triggers every moult; on its own it would take the caterpillar straight to the adult form. Juvenile hormone, from a pair of glands behind the brain, holds that back, and while it is present each moult produces another, larger caterpillar. When the larva has reached the right size, the juvenile hormone switches off, and the next surge of ecdysone starts the pupa instead. Experiments that keep juvenile hormone flowing produce giant caterpillars that never pupate, and the insecticides that mimic it work by trapping pests in a larval stage they cannot leave.

Not everything dissolves. The nervous system is remodelled rather than replaced, and enough survives that some memories cross over. In 2008 researchers trained caterpillars of the tobacco hornworm to avoid a particular smell by pairing it with a mild electric shock, and the moths that emerged weeks later still avoided it, provided the training had happened late in larval life. The gut is rebuilt around the old one, the breathing tubes are retained and extended, and some larval muscles are kept and reworked. The animal that flies away is genetically identical to the one that crawled in and carries a few of its lessons, but in most of its body it is new.

Complete metamorphosis appeared around 300 million years ago and turned out to be the most successful body plan on land: some four fifths of all insect species, and so the majority of all known animals, go through it. The advantage is that a single genome can run two specialists in sequence, a feeding machine and a flying, mating machine, each free to be shaped by evolution for its one job without compromising the other. Grasshoppers, dragonflies and cockroaches do it the older way, hatching as small versions of the adult and growing by stages, which is cheaper but makes the young and the old compete for the same food. The caterpillar and the butterfly are the same animal that has agreed, for a few weeks in a hard case, to become someone else.

The words chrysalis and cocoon are often used as if they meant the same thing, but they describe different objects. A chrysalis is the pupa of a butterfly itself: the hardened outer skin of the animal, hanging bare from a silk pad. A cocoon is a separate case of silk that many moth caterpillars spin around themselves before they pupate, so the pupa sits inside a wrapping it made. The silk of the domesticated silkworm, a moth, comes from unwinding exactly such cocoons. Some moths skip the silk altogether and pupate in a small chamber in the soil.

A second mix-up concerns which animals count as caterpillars. Sawfly larvae, which feed on leaves of roses, willows and pine trees, look very like caterpillars but belong to the same group as bees and wasps. One way to tell them apart is to count the fleshy legs along the belly behind the three pairs of true legs: butterfly and moth caterpillars have at most five pairs, while sawfly larvae usually have six or more. The resemblance is a case of similar lifestyles producing similar bodies in unrelated animals, since a leaf-eating tube with legs works well whichever insect grows into it.

If you raise butterflies at home from a kit, you can watch the final stage closely. A day or so before emergence the chrysalis of many species darkens or turns see-through as the adult's colours show through the thin case. The butterfly usually breaks out in the morning, clings to the empty shell and pumps its wings full. Within a few hours it also squirts out a drop or two of reddish fluid. This is meconium, the waste left over from building the adult inside the chrysalis, and newcomers often panic that the insect is bleeding. It is perfectly normal.

Those drops have a small place in the history of science. Medieval and early modern Europe recorded many rains of blood, red spots appearing overnight on walls and stones, which were often read as omens. In 1608, after such a shower alarmed people in Provence, the French scholar Nicolas-Claude Fabri de Peiresc investigated. He had kept a chrysalis himself and seen the emerging butterfly leave a red drop, and he noticed that the spots appeared in sheltered places where rain could not have fallen. He concluded that a mass emergence of butterflies, not a miracle, explained the blood.

Monarch butterflies in eastern North America make one of the most remarkable insect migrations, and it depends on a change in their life cycle. Most monarchs live only a few weeks as adults, and several generations are born over a summer as the population spreads north. The last generation of the year, emerging in late summer, is different.

These butterflies delay breeding and can live for around eight months, flying thousands of kilometres south to overwintering forests in the mountains of central Mexico, where millions cluster on fir trees. In spring they head north and lay eggs, and their descendants complete the return over several generations. No individual makes the full round trip, so the route is inherited rather than learned, one of the great puzzles of animal navigation.

Inside the chrysalis a caterpillar dissolves most of its own tissues and builds the adult from imaginal discs, small groups of cells carried since the embryo that each grow into a wing, leg, eye or antenna, using the dissolved larva as raw material. The switch from larval moults to pupation is made when juvenile hormone stops, the nervous system and some memories survive the rebuild, and the whole arrangement lets one genome run two specialised animals in turn.