How Does a Caterpillar Become a Butterfly? What Happens Inside the Chrysalis
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Cut open a chrysalis a few days after it forms and there is no half-made butterfly inside, only a thick fluid with a few structures floating in it. The caterpillar has taken itself apart. Most of its tissues have been dissolved into a soup of cells and nutrients, and the adult is being built from small groups of cells that had been waiting, unused, since the animal was an egg. The process is called complete metamorphosis, it is shared by beetles, bees, flies and moths, and it is one of the strangest things an animal does.
Two animals in one life
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.
Inside the chrysalis
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
The hormone that decides
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.
What the butterfly remembers
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.
Why do it this way
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 takeaway
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.