|Luna Moth (Source)|
Blackiston et al., (2008) from Georgetown University designed an experiment to test exactly that question.
They exposed caterpillars to a specific smell and then gave them an electric shock. They then tested the caterpillar's aversion to the smell by letting it run around in a Y shaped structure. One arm had the 'scary smell' and the other just had normal air.
|Blackiston et al. 2008 figure 1|
After the caterpillars had learned that the smell predicted an electric shock, they preferred the ambient air arm compared to the 'scary smell' arm. Specifically 78% of the caterpillars spent more time in the ambient air arm.
So, great, caterpillars can learn to avoid a smell. Not super exciting on its own. The real test was to train the creature as a caterpillar and then test the creature as a moth.
And indeed, the moths remembered. 80% of adult moths chose the ambient air over the 'scary smell' air. Interestingly, the moths only remembered if they were trained late in their caterpillar life, but not if they were trained as very young caterpillars.
So what does this mean? Well, like most fascinating scientific findings, it raises many questions. In particular it makes me wonder what exactly is happening in the brain during metamorphosis?
Are the neurons even firing? Do they go into some kind of paused-frozen state?
I haven't heard of anyone recording the electrical signals from neurons or imaging the calcium dynamics of pupal moths or butterflies, but I think this would be a great experiment.
Clearly the caterpillar isn't completely destroyed and rebuilt, some components persist. The specific synaptic connections that encode the connection between the smell and the scariness must be maintained.
And of course this answers the longstanding literary question of how exactly Gregor Samsa can remember who he is after he transforms into a cockroach.
Blackiston DJ, Silva Casey E, & Weiss MR (2008). Retention of memory through metamorphosis: can a moth remember what it learned as a caterpillar? PloS one, 3 (3) PMID: 18320055