Continuously fluctuating selection reveals extreme granularity and parallelism of adaptive tracking

Temporally fluctuating environmental conditions are a ubiquitous feature
of natural habitats. Yet, how finely natural populations adaptively track
fluctuating selection pressures via shifts in standing genetic variation
is unknown. We generated high-frequency, genome-wide allele frequency data
from a genetically diverse population of Drosophila melanogaster in
extensively replicated field mesocosms from late June to mid-December, a
period of ~12 generations. Adaptation throughout the fundamental
ecological phases of population expansion, peak density, and collapse was
underpinned by extremely rapid, parallel changes in genomic variation
across replicates. Yet, the dominant direction of selection fluctuated
repeatedly, even within each of these ecological phases. Comparing
patterns of allele frequency change to an independent dataset procured
from the same experimental system demonstrated that the targets of
selection are predictable across years. In concert, our results reveal
fitness-relevance of standing variation that is likely to be masked by
inference approaches based on static population sampling, or
insufficiently resolved time-series data. We propose such fine-scaled
temporally fluctuating selection may be an important force maintaining
functional genetic variation in natural populations and an important
stochastic force affecting levels of standing genetic variation
genome-wide.