The Genetic Architecture Underlying Rapid Seasonal Evolution in Natural Populations of Drosophila Melanogaster

The rate and tempo at which populations respond to environmental change is fundamental in understanding the adaptive process. Evolution is generally considered to be a gradual process and it is unclear if populations can adapt rapidly to environmental selection pressures. Annual seasonal rhythms produce rapid, predictable environmental changes that may result in rapid adaptation in multivoltine species that reproduce multiple times each year. This work demonstrates that Drosophila melanogaster adapts rapidly and predictably to seasonal environmental changes across five years and multiple locations. Suites of complex fitness traits change in a predictable way over the 10–15 generations from spring to fall. After surviving the harsh environmental selection of the winter, the spring flies are characterized by a increased investment in somatic maintainance: higher resistance to thermal stress, higher tolerance to pathogenic infection, faster development time and better learning. These traits decline throughout the summer when ripening fruit is abundant due to correlated trade-offs with reproduction. Parallel changes in G-matrixes over this seasonal timescale counters the basic assumption of stable covariance over time and indicates that selection acts rapidly to alter the genetic architecture of a population. We show that there are alleles that have functional effects on these important life history traits that oscillate in frequency as a function of seasonal time, but that non-additive epistatic interactions are prevalent and shape the genetic architecture of change across seasonal time. Functional analysis of candidate genes shows that epistatic interactions among seasonally oscillating alleles facilitate rapid adaptation by producing emergent fitness phenotypes. Together, these findings demonstrate rapid, repeatable adaptation to abiotic and biotic environmental parameters that cycle as a function of seasonal time. Epistatic interactions within and among genes facilitate the rapid evolutionary change that is occurring over timescales previously considered static