A genotype-phenotype-fitness map reveals local modularity and global pleiotropy of adaptation

Building a genotype to phenotype to fitness map of adaptation is a central goal in evolutionary biology. It is also notoriously difficult even when the adaptive mutations are known because it is hard to identify which phenotypes make these mutations adaptive. We solve this problem by first quantifying how the fitness of hundreds of adaptive mutants responds to subtle environmental shifts and then inferring the existence of fitness-relevant phenotypes implicit in these patterns of fitness variation. We find that a small number of phenotypes predicts the fitness of the adaptive mutations near their original glucose-limited evolution condition. Importantly, phenotypes that matter little to fitness at or near the evolution condition can matter strongly in distant environments. This suggests that adaptive mutants are locally modular - affecting a small number of phenotypes that matter to fitness in the environment where they evolve - yet globally pleiotropic - affecting many phenotypes that contribute to fitness in new environments.

构建适应性研究中从基因型到表型再到适应度的映射关系，是进化生物学的核心研究目标之一。即便已知适应性突变的具体信息，实现该目标仍极具挑战性——这是由于我们难以确定究竟是哪些表型赋予了这些突变适应性优势。本研究通过两步路径解决该难题：首先量化数百个适应性突变体的适应度对细微环境变化的响应模式，随后基于这些适应度变异的特征分布，推断出隐含其中的、与适应度相关的表型的存在。研究发现，在适应性突变体最初演化所处的葡萄糖限制培养环境及其邻近环境中，仅需少量表型即可准确预测这些突变体的适应度。值得注意的是，在演化环境或其邻近环境中对适应度影响微弱的表型，在差异显著的远端环境中却可对适应度产生强烈作用。这一结果表明，适应性突变体兼具两种特性：在其自身演化的环境中呈现局部模块化特征——仅影响少数与适应度相关的表型；而在全新环境中则表现为全局多效性——会影响诸多与适应度相关的表型。