Do Butterflies or Moths Retain Memories from Their Caterpillar Stage?

演化之聲
Mar 13
4 min read

Insects that undergo complete metamorphosis experience dramatic transformations throughout their life cycle. The transition from larva to pupa and finally to adult involves not only profound morphological change but also extensive reorganization of tissues and organs. At first glance, such a process appears so radical that it seems unlikely that anything from the larval stage could persist into adulthood, particularly elements of the nervous system. Yet some research has suggested that experiences acquired during the larval stage may influence adult behavior. This possibility raises a fundamental question: can memories formed during the larval stage survive metamorphosis and remain accessible in the adult insect?

To investigate this question, researchers studied the tobacco hornworm moth, Manduca sexta. The experiment examined whether caterpillars that learned to avoid a particular odor during the larval stage would retain this avoidance behavior after metamorphosis. Third-instar and fifth-instar larvae were exposed to the odor of ethyl acetate while simultaneously receiving a mild electric shock. Each caterpillar underwent eight such conditioning trials in a single day. The pairing of odor and shock was intended to create an associative learning experience in which the larvae would learn to avoid the odor.

After training, the larvae were tested in a Y-shaped apparatus. One arm of the apparatus carried air containing the odor of ethyl acetate, while the other arm contained clean air. By observing which arm the caterpillar chose, researchers could determine whether the larvae had learned to avoid the odor. The results showed that trained larvae indeed developed an aversion to the odor and tended to move toward the arm containing clean air.

The crucial question, however, was whether this learned behavior would persist after the insects completed metamorphosis and emerged as adult moths. Once the trained larvae pupated and later eclosed as adults, they were tested again in the same Y-shaped apparatus. Interestingly, the outcome depended on the developmental stage at which the training occurred.

When larvae had been trained during the fifth instar, the resulting adult moths continued to avoid the odor of ethyl acetate. In other words, the memory formed during the larval stage survived the pupal transformation and influenced behavior in the adult stage. In contrast, larvae that had been trained earlier, during the third instar, did not display odor avoidance as adults. Although these individuals still avoided the odor during the larval period, the memory disappeared during metamorphosis and did not carry over into the adult stage.

Statistics of odor avoidance behavior in adults: Untreated (untrained control group), Shock only, Odor only, Shock+Odor, 5th instar (fifth-instar larvae conditioned with shock and odor), Shock+Odor, 3rd instar (third-instar larvae conditioned with shock and odor)（圖片來源：Blackiston JD et al，採用 CC BY 3.0 授權）

These findings suggest that the persistence of memory through metamorphosis may depend on when the learning occurs during larval development. A key factor appears to be the development of specific neural structures in the insect brain known as the mushroom bodies. These paired brain regions play a central role in learning and memory in many insects. The mushroom bodies contain several subdivisions, including the calyx and multiple lobes designated α/β, α′/β′, and γ.

The γ lobe forms early in development and undergoes extensive remodeling during metamorphosis. Many of its synaptic connections are pruned as the nervous system reorganizes, which likely erases memories associated with this region. By contrast, the α′/β′ lobes develop later and remain largely intact during metamorphosis. Memories stored in circuits associated with these later-forming regions may therefore persist into adulthood.

This developmental pattern provides a possible explanation for the experimental results. Memories acquired during the third instar may rely on neural structures that are subsequently reorganized or removed during pupation. Consequently, those memories are lost by the time the insect becomes an adult. Memories formed during the fifth instar, however, may involve neural circuits that remain stable through metamorphosis, allowing the information to persist.

The ability to retain memories across metamorphosis could have important ecological consequences. For example, adult moths often choose specific plants on which to lay their eggs. If a moth retains information about the plant species it fed on as a caterpillar, it may preferentially select that same plant as an oviposition site. Such behavior would ensure that the next generation of larvae encounters a suitable food source immediately after hatching.

This phenomenon also has broader implications for insect evolution. If larval experiences influence adult habitat choice or host-plant preference, populations feeding on different plants could gradually diverge. Over time, such behavioral differences could contribute to the formation of host races and potentially even lead to speciation.

These findings challenge the long-standing popular notion that metamorphosis completely dismantles the caterpillar and rebuilds it into a butterfly or moth. Although extensive remodeling certainly occurs, parts of the nervous system can remain functionally continuous across developmental stages. The persistence of memory through metamorphosis suggests that the transformation is not a complete reset of the organism, but rather a complex reorganization in which certain neural circuits and learned experiences can survive the transition.