Data from: Genomic evidence of rapid and stable adaptive oscillations over seasonal time scales in Drosophila

In many species, genomic data have revealed pervasive adaptive evolution indicated by the fixation of beneficial alleles. However, when selection pressures are highly variable along a species' range or through time adaptive alleles may persist at intermediate frequencies for long periods. So called “balanced polymorphisms” have long been understood to be an important component of standing genetic variation, yet direct evidence of the strength of balancing selection and the stability and prevalence of balanced polymorphisms has remained elusive. We hypothesized that environmental fluctuations among seasons in a North American orchard would impose temporally variable selection on Drosophila melanogaster that would drive repeatable adaptive oscillations at balanced polymorphisms. We identified hundreds of polymorphisms whose frequency oscillates among seasons and argue that these loci are subject to strong, temporally variable selection. We show that these polymorphisms respond to acute and persistent changes in climate and are associated in predictable ways with seasonally variable phenotypes. In addition, our results suggest that adaptively oscillating polymorphisms are likely millions of years old, with some possibly predating the divergence between D. melanogaster and D. simulans. Taken together, our results are consistent with a model of balancing selection wherein rapid temporal fluctuations in climate over generational time promotes adaptive genetic diversity at loci underlying polygenic variation in fitness related phenotypes.

在诸多物种中，基因组数据已揭示了广泛存在的适应性演化，其标志性表现为有益等位基因（beneficial allele）的固定。然而，当选择压力在物种分布范围内随空间或随时间发生剧烈波动时，适应性等位基因可能会长时间以中等频率存续。长期以来，人们认为平衡多态性（balanced polymorphisms）是现存遗传变异的重要组成部分，但有关平衡选择强度、平衡多态性的稳定性与普遍性的直接证据却始终难以获取。我们提出假说：北美一处果园内的季节环境波动，会对黑腹果蝇（Drosophila melanogaster）施加随时间变化的选择压力，进而推动平衡多态性位点出现可重复的适应性频率振荡。我们共鉴定出数百个频率随季节振荡的多态性位点，并认为这些基因座（locus）受到强烈且随时间波动的选择作用。我们证实，这些多态性位点会响应气候的突发性与持续性变化，并与随季节变化的表型以可预测的方式相关联。此外，我们的研究结果表明，发生适应性频率振荡的多态性位点可能已有数百万年的演化历史，其中部分位点的起源甚至早于黑腹果蝇与拟果蝇（Drosophila simulans）的分化事件。综合来看，我们的研究结果与平衡选择模型相符：在世代尺度上，气候的快速时间波动会促进与适合度相关表型的多基因变异所依托的基因座的适应性遗传多样性。