Abstract
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.
Impact statement Evolution is traditionally considered to be a very slow, gradual process, but recent studies show that some organisms evolve rapidly for a variety of traits. However, there is still little known about the rate at which behaviors evolve in the wild. Complex behaviors may evolve due to their fitness benefits or because natural selection acts on a trait that is genetically correlated with that behavior. Learning ability is an important behavior for many aspects of an organism’s biology, but may be costly and use resources that could be otherwise allocated to other important functions, such as reproduction. We measure learning ability in fruit flies collected from a natural population as it evolves across seasons. We find that the complex behavior of learning ability evolves very fast the wild at the cost of reproduction: the spring populations have higher learning ability but lay fewer eggs compared to the fall. We found that natural variants of the couch potato help mediate the trade-off between reproduction and learning in natural populations. This shows how evolution of complex traits can occur due to selection on genes that affect multiple traits.
