“Insects that undergo complete metamorphosis, such as moths and butterflies, retain memories and learned behaviors acquired during their larval (caterpillar) stage after transforming into adults.”

The tobacco hornworm, Manduca sexta, provides an intermediate case in which both larva and adult possess functional, but quite different legs. Embryonic patterning of the leg bud progresses through a basal ring of dachshund expression and a single bric-a-brac domain but then arrests and directs the development of a caterpillar leg. As in Drosophila, though, the patterning sequence is eventually completed at metamorphosis to make the adult leg.

The present study, the first to demonstrate conclusively that associative memory survives metamorphosis in Lepidoptera, provokes intriguing new questions about the organization and persistence of the central nervous system during metamorphosis. Our results have both ecological and evolutionary implications, as retention of memory through metamorphosis could influence host choice by polyphagous insects, shape habitat selection, and lead to eventual sympatric speciation. We show that larvae learned to avoid the training odor, and that this aversion was still present in the adults.

The present study, the first to demonstrate conclusively that associative memory survives metamorphosis in Lepidoptera, provokes intriguing new questions about the organization and persistence of the central nervous system during metamorphosis. We show that larvae learned to avoid the training odor, and that this aversion was still present in the adults. The adult aversion did not result from carryover of chemicals from the larval environment, as neither applying odorants to naïve pupae nor washing the pupae of trained caterpillars resulted in a change in behavior.

We have demonstrated that M. sexta larvae can learn to associate odor cues with an aversive stimulus, and that this memory persists undiminished across two larval molts, as well as into adulthood. The behavior represents true associative learning, not chemical legacy, and, as far as we know, provides the first definitive demonstration that associative memory survives metamorphosis in Lepidoptera.

Our failure to find anatomical support in Drosophila for persistence of a memory trace from larva to adult should not be generalized to other insects with a larval stage. There is evidence that associative learning in moth caterpillars and beetle grubs can carry through to the adult (Blackiston et al., 2015; Blackiston et al., 2008). Larvae of butterflies and beetles have an extended embryonic development compared to Drosophila, and they hatch with a more complex larval nervous system.

In heterometabolous insects, larval personality (e.g. boldness) generally persists at the adult stage. However, either mean value of the trait decreases, with larvae being bolder than adults, or the mean value is maintained only in females.

These results indicate that G. molesta larvae are able to associate an olfactory stimulus (ethyl acetate odour) with an aversive stimulus (electric shock) and that the aversive memory established is maintained 24 hours after training and even 72 hours after metamorphosis. Thus, G. molesta has the ability to associate an odour to an aversive stimulus precociously, and this association is maintained through metamorphosis and persists into adulthood.

The reshuffling of neurons during fruit fly metamorphosis suggests that larval memories don't persist in adults. They found that, unlike the tormented protagonist of Franz Kafka’s short story “The Metamorphosis,” who awakes one day as a monstrous insect, adult insects likely can’t remember much of their larval life. Although many of the larval neurons in the study endured, the part of the insect brain that Truman’s group examined was dramatically rewired.

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. 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.

When the larvae turned into adult moths, most continued to avoid the odour, suggesting that moths and butterflies may indeed remember some of their larval experiences. The transition from caterpillar to butterfly via a soupy pupal mashup remains one of the greatest mysteries of the animal kingdom. During metamorphosis, body parts are liquified and then reorganised, but the ability of memories to survive this process was unknown.

After attaining MVW, larvae pass another checkpoint, critical weight (CW), defined as the minimum larval size at which starvation no longer delays the larval-adult transition. This describes developmental checkpoints but does not address memory retention.

The combination of cell death, compartment shifting, trans-differentiation, and recruitment of new neurons result in no larval MBIN-MBON connections being maintained through metamorphosis. At this simple level, then, we find no anatomical substrate for a memory trace persisting from larva to adult.

They found that, unlike the tormented protagonist of Franz Kafka’s short story “The Metamorphosis,” who awakes one day as a monstrous insect, adult insects likely can’t remember much of their larval life. Although many of the larval neurons in the study endured, the part of the insect brain that Truman’s group examined was dramatically rewired. The reshuffling of neurons during fruit fly metamorphosis suggests that larval memories don't persist in adults.

In another experiment, designed to determine whether a learned memory could persist across the dramatic changes of complete metamorphosis, Dr. Weiss began by training caterpillars to avoid a particular odor. Interestingly, her experiment showed that moths do retain memories learned as a caterpillar. The moths that she and her team had trained six weeks before still knew to avoid that odor.

While the claim is largely supported by research on Lepidoptera (moths and butterflies), the extent and mechanisms of memory retention can vary across different orders of holometabolous insects. Studies on some species, like certain fruit flies (Drosophila), suggest significant neural rewiring during metamorphosis that may limit the carryover of complex associative memories, even if some neurons persist.