The transformation from caterpillar to butterfly or moth is one of the most beguiling in the animal world. Both larva and adult are just stages in the life of a single animal, but are nonetheless completely separated in appearance, habitat and behaviour. The imagery associated with such change is inescapably beautiful, and as entrancing to a poet as it is to a biologist.
According to popular belief, within the pupa, the caterpillar's body is completely overhauled, broken down into a form of soup and rebuilt into a winged adult. Richard Buckmister Fuller once said that "there is nothing in a caterpillar that tells you it's going to be a butterfly." Indeed, as the butterfly or moth quite literally flies off into a new world, it is tempting to think that there is no connection between its new life and its old existence as an eating machine. But not so. A new study has provided strong evidence that the larval and adult stages are not as disparate as they might seem. Adult tobacco hookworms - a species of moth - can remember things that it learned as a caterpillar, which means that despite the dramatic nature of metamorphosis, some elements of the young insect's nervous system remain intact through the process.
Using some mild electric shocks, Douglas Blackiston from Georgetown University trained hookworm caterpillars (Manduca sexta) to avoid the scent of a simple organic chemical - ethyl acetate. The larvae were then placed in the bottom end of a Y-shaped tube, with the scent of ethyl acetate wafting down one arm and fresh air coming down the other. Sure enough, 78% of the trained caterpillars inched down the odour-free arm.
As the caterpillar moulted their way through the larval stage, their aversion to ethyl acetate remained. Blackiston allowed them to pupate and emerge as full-grown moths, before testing them again, about a month after their initial 'electric' education. Bear in mind that a tobacco hornworm lives for about 30 to 50 days, so a month is very close to its entire lifespan.
Amazingly, 77% of the adult moths also avoided the ethyl acetate-scented arm of the Y-shaped tube and the vast majority of these were the adult versions of the same larvae that had correctly learned the behaviour originally. Clearly, the larvae had learned to avoid the chemical and that memory carried over into adulthood.
Even so, Blackiston was careful to rule out alternative explanations. For a start, ethyl acetate isn't naturally foul-smelling. It's actually rather reminiscent of pear drops and when larvae are exposed to it in the absence of electric shocks, neither they nor the adults they become learn to avoid it.
Another possible explanation hinges on the fact that adults emerging from the pupa usually experience a similar milieu of smells to their caterpillar selves. This chemical legacy' could explain why adults and larvae react similarly to some odours. But when Blackiston applied ethyl acetate gel to the pupae of untrained caterpillars, the adults did not shrink away from the chemical. Nor did washing the pupae of trained caterpillars, to get rid of any lingering traces of ethyl acetate, have any effect.
How and why?
Blackiston was convinced that some aspect of the caterpillar' nervous system was carried over into adulthood. However, he also found that this only happened if caterpillars are trained at the last possible stage before they pupate - the 'fifth instar'. Any earlier, and the memories don't stick.
The fruitfly Drosophila suggests why this might happen. In its brain, memories of smells are located in mushroom bodies, brain structures that consist of three lobes. The gamma lobe develops very early while the alpha and beta lobes develop just before the pupal stage.
Blackiston thinks that long-lasting larval memories are writ into the alpha and beta lobes, whose neural networks are kept around while the rest of the caterpillar breaks down. If the larvae are too young, these areas haven't developed yet and any learned information is stored in the gamma lobe and lost when its connections are trimmed back in the pupa.
But why bother? After all, the entire advantage of metamorphosis rests on the very different lifestyles and habitats of caterpillars and moths, which allow them to avoid competing with each other. Nonetheless, moths and butterflies must still return to the right sort of plant in order to lay their eggs and Blackiston suggests that their larva-hood memories may help them to do so.
Images by Kugamazog and Xfigpower, from Wikipedia
Reference: Blackiston, D.J., Silva Casey, E., Weiss, M.R., Healy, S. (2008). Retention of Memory through Metamorphosis: Can a Moth Remember What It Learned As a Caterpillar?. PLoS ONE, 3(3), e1736. DOI: 10.1371/journal.pone.0001736