Natural variation in couch potato mediates rapid evolution of learning and reproduction in natural populations of Drosophila melanogaster

Seasonal oscillations in temperate environments between the different selection regimes of winter and summer produce cyclical selection pressures that may drive rapid evolution of diverse traits. We investigated the evolutionary dynamics of learning ability in natural populations over this rapid seasonal timescale. Associative learning was tested in common garden-raised Drosophila melanogaster collected from a natural population in the spring and fall over three consecutive years. The spring flies learned consistently better than fall flies, revealing seasonal evolution of improved learning performance in nature. Fecundity showed the opposite seasonal pattern, suggesting a trade-off between learning and reproduction, which we confirmed at the level of individual females. This trade-off is mediated at least in part by natural polymorphism in the RNA binding protein couch potato (cpo), with a haplotype favored during summer showing poorer learning performance and higher fecundity than a haplotype favored over winter. Thus, seasonal environments can drive rapid cyclical evolution of learning performance, but the evolutionary dynamics may be driven by pleiotropic effects of alleles selected for other reasons.