Species differences in learning about gustatory and visual stimuli in two recently diverged species of Drosophila

Learning is central to our understanding of how behaviour is shaped by the environment. A key open question is whether learning across contexts evolves as an integrated process, or whether learning in each context is free to evolve separately. Here, we measured learning in two sensory contexts in multiple genotypes and both sexes of two closely related, but ecologically divergent, species of fruit flies, Drosophila simulans and Drosophila sechellia. These species are morphologically very similar but differ dramatically in ecology and population biology. We tested how flies from each genotype, sex and species responded to and learned about different gustatory and visual cues. This approach allowed us to test whether species differences in learning were independent or correlated across contexts. Surprisingly, we found no evidence that D. simulans learned in any of our treatments. In contrast, D. sechellia learned to avoid gustatory stimuli that were paired with an aversive stimulus, as predicted, but unexpectedly learned to approach visual stimuli that were paired with the aversive stimulus. At the genotype level, genotypes, but not species, differed in their naïve responses to stimuli, but genotypes did not differ in learning in either species. Our results demonstrate that D. sechellia indeed differs from D. simulans in both learning contexts, but in a stimulus-dependent way. We suggest that studies of additional species or population pairs that employ this framework will be critical for evaluating the dimensionality of learning and its evolution.