Genetic redundancy fuels polygenic adaptation in Drosophila

The genetic architecture of adaptive traits is of key importance to predict evolutionary responses. Most adaptive traits are polygenic—i.e., result from selection on a large number of genetic loci—but most molecularly characterized traits have a simple genetic basis. This discrepancy is best explained by the difficulty in detecting small allele frequency changes (AFCs) across many contributing loci. To resolve this, we use laboratory natural selection to detect signatures for selective sweeps and polygenic adaptation. We exposed 10 replicates of a Drosophila simulans population to a new temperature regime and uncovered a polygenic architecture of an adaptive trait with high genetic redundancy among beneficial alleles. We observed convergent responses for several phenotypes—e.g., fitness, metabolic rate, and fat content—and a strong polygenic response (99 selected alleles; mean s = 0.059). However, each of these selected alleles increased in frequency only in a subset of the evolving replicates. We discerned different evolutionary paradigms based on the heterogeneous genomic patterns among replicates. Redundancy and quantitative trait (QT) paradigms fitted the experimental data better than simulations assuming independent selective sweeps. Our results show that natural D. simulans populations harbor a vast reservoir of adaptive variation facilitating rapid evolutionary responses using multiple alternative genetic pathways converging at a new phenotypic optimum. This key property of beneficial alleles requires the modification of testing strategies in natural populations beyond the search for convergence on the molecular level.

适应性性状的遗传架构对于预测进化响应至关重要。多数适应性性状属于多基因性状——即由大量遗传位点上的选择作用塑造而成——但目前在分子层面已被表征的性状大多仅具备简单的遗传基础。这种差异最合理的解释是，难以在众多贡献位点中检测到微小的等位基因频率变化（AFCs）。为解决这一难题，我们借助实验室自然选择来检测选择性清除与多基因适应的特征信号。我们将10个重复的拟果蝇（Drosophila simulans）种群暴露于全新的温度环境中，揭示了一类适应性性状的多基因遗传架构，其有益等位基因间存在高度遗传冗余现象。我们观察到多个表型出现趋同响应——例如适合度、代谢速率与脂肪含量——同时检测到强烈的多基因响应（共99个受选择等位基因；平均选择系数s=0.059）。然而，每一个受选择等位基因仅在部分进化重复种群中发生频率上升。我们基于各重复种群间的异质性基因组模式，识别出不同的进化范式。相较于假设独立选择性清除的模拟结果，遗传冗余与数量性状（QT）范式更契合本实验的数据。我们的研究结果表明，天然拟果蝇种群蕴藏着丰富的适应性变异储备，可通过多条替代遗传通路快速产生进化响应，最终收敛至新的表型最适状态。有益等位基因的这一关键特性，要求我们对自然种群的检测策略进行修正，不再仅局限于分子层面的趋同性搜索。