Rapid evolution of learning and reproduction in natural populations of Drosophila melanogaster

Abstract

Learning is a general mechanism of adaptive behavioural plasticity whose benefits and costs depend on the environment. Seasonal oscillations in temperate environments between winter and summer produce cyclical selection pressures that may drive rapid evolution of learning performance in multivoltine populations. To test this hypothesis, we investigated the evolutionary dynamics of learning ability over rapid seasonal timescales in a natural population of Drosophila melanogaster. Associative learning was tested in common-garden-raised flies collected in the spring and autumn over three consecutive years. Spring flies consistently learned better than autumn flies, revealing seasonal evolution of improved learning performance in nature. Fecundity showed the opposite seasonal pattern, suggesting a trade-off between learning and reproduction that also held 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): a genotype favoured during summer showed poorer learning performance and higher fecundity than a genotype favoured over winter. Thus, seasonal environments can drive rapid cyclical evolution of learning performance, but the evolutionary dynamics may be driven by trade-offs generated by pleiotropic effects of causative alleles selected for other reasons.