Large-effect flowering time mutations reveal conditionally adaptive paths through fitness landscapes in Arabidopsis thaliana

First author: Mark A. Taylor; Affiliations: University of California, Davis (加利福尼亚大学戴维斯分校): CA, USA

Corresponding author: Johanna Schmitt

Contrary to previous assumptions that most mutations are deleterious, there is increasing evidence for persistence of large-effect mutations in natural populations. A possible explanation for these observations is that mutant phenotypes and fitness may depend upon the specific environmental conditions to which a mutant is exposed. Here, we tested this hypothesis by growing large-effect flowering time mutants of Arabidopsis thaliana in multiple field sites and seasons to quantify their fitness effects in realistic natural conditions. By constructing environment-specific fitness landscapes based on flowering time and branching architecture, we observed that a subset of mutations increased fitness, but only in specific environments. These mutations increased fitness via different paths: through shifting flowering time, branching, or both. Branching was under stronger selection, but flowering time was more genetically variable, pointing to the importance of indirect selection on mutations through their pleiotropic effects on multiple phenotypes. Finally, mutations in hub genes with greater connectedness in their regulatory networks had greater effects on both phenotypes and fitness. Together, these findings indicate that large-effect mutations may persist in populations because they influence traits that are adaptive only under specific environmental conditions. Understanding their evolutionary dynamics therefore requires measuring their effects in multiple natural environments.

之前多认为大多数的突变是有害的，然而越来越多的证据显示在自然群体中往往会持续存在效应较大的突变。对于这种现象可能的解释之一就是突变表型和适应性可能依赖于突变体所处的特定环境条件。本文中，作者通过在多个大田试验点、多个季节种植效应较大的开花时间拟南芥突变体测试该理论，定量这些突变体在真实的环境条件下的适应性。基于开花时间和分枝结构，作者绘制了特定环境下突变体的适应性图谱，结果显示有一些突变体的适应性增强，但仅限于特定的环境条件下。这些突变体通过多个途径增加植株的适应性，或是通过开花时间的改变，或是通过分枝的改变，抑或是二者的共同作用。分枝受到了更强的选择，但开花时间的遗传变异更大，说明突变对于多个表型的多效性影响对于突变的间接选择十分重要。最后，作者还发现调控网络中往往居于中心的、具有更高连通性的关键基因的突变对于表型和适应的影响更大。综上，本文的研究揭示了效应较大的突变在自然群体中持续存在可能与其影响植株在特定环境条件下的适应性相关。另外，为了理解这些突变在演化历史中的作用，作者认为需要在多个自然环境条件下测试他们所造成的影响。

通讯：Johanna Schmitt  (https://biology.ucdavis.edu/people/johanna-schmitt)

个人简介：1974年，斯沃斯摩尔学院，学士；1981年，斯坦福大学，博士。

研究方向：植物生态基因组学和演化生态学；表型可塑性、地域适应和对环境变化的响应机制。

doi: https://doi.org/10.1073/pnas.1902731116

Journal: PNAS

First Published: August 16, 2019