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.

随时间波动的环境条件是自然栖息地普遍存在的特征。然而，自然种群如何通过现存遗传变异（standing genetic variation）的改变，自适应地追踪波动的选择压力，目前仍未有定论。我们以遗传多样性丰富的黑腹果蝇（Drosophila melanogaster）种群为研究对象，在高度重复的野外中型实验生态系统（field mesocosms）中，于6月末至12月中旬（时长约12个世代）采集了高频全基因组等位基因频率数据。在种群扩张、密度峰值及种群衰退这三大核心生态阶段中，适应过程均依托于各重复组间基因组变异的极快速平行变化。但即便在上述任一生态阶段内部，选择的主导方向也会反复发生波动。将等位基因频率变化模式与同一实验系统获取的独立数据集进行比对后发现，选择的作用靶点在不同年份间具备可预测性。综合而言，本研究结果揭示了现存遗传变异的适合度相关性——这类变异很可能会被基于静态种群采样或分辨率不足的时间序列数据的推断方法所遮蔽。我们认为，这种精细尺度的随时间波动的选择作用，或许是维持自然种群中功能性遗传变异的重要动力，同时也是影响全基因组现存遗传变异水平的关键随机驱动力。