Data from: Foraging environment determines the genetic architecture and evolutionary potential of trophic morphology in cichlid fishes

Phenotypic plasticity allows organisms to change their phenotype in response to shifts in the environment. While a central topic in current discussions of evolutionary potential, a comprehensive understanding of the genetic underpinnings of plasticity is lacking in systems undergoing adaptive diversification. Here, we investigate the genetic basis of phenotypic plasticity in a textbook adaptive radiation, Lake Malawi cichlid fishes. Specifically, we crossed two divergent species to generate an F3 hybrid mapping population. At early juvenile stages, hybrid families were split and reared in alternate foraging environments that mimicked benthic/scraping or limnetic/sucking modes of feeding. These alternate treatments produced a variation in morphology that was broadly similar to the major axis of divergence among Malawi cichlids, providing support for the flexible stem theory of adaptive radiation. Next, we found that the genetic architecture of several morphological traits was highly sensitive to the environment. In particular, of 22 significant quantitative trait loci (QTL), only one was shared between the environments. In addition, we identified QTL acting across environments with alternate alleles being differentially sensitive to the environment. Thus, our data suggest that while plasticity is largely determined by loci specific to a given environment, it may also be influenced by loci operating across environments. Finally, our mapping data provide evidence for the evolution of plasticity via genetic assimilation at an important regulatory locus, ptch1. In all, our data address long-standing discussions about the genetic basis and evolution of plasticity. They also underscore the importance of the environment in affecting developmental outcomes, genetic architectures, morphological diversity and evolutionary potential.

表型可塑性（phenotypic plasticity）指生物体可随环境变化改变自身表型。尽管其是当前进化潜力讨论的核心议题，但对于正经历适应性分化的类群，学界仍缺乏对可塑性遗传基础的全面认知。本研究以马拉维湖慈鲷这一教科书中典型的适应性辐射类群为对象，解析其表型可塑性的遗传机制。我们通过杂交两个分化程度迥异的物种，构建了F3杂交作图群体。在幼体早期，将杂交家系分组饲养于两种对照环境中，分别模拟底栖刮食与浮游吮吸的摄食模式。这两种环境处理诱导产生的形态变异，与马拉维湖慈鲷类群间的主要分化轴高度吻合，为适应性辐射的灵活茎理论提供了实证支持。进一步研究发现，多项形态性状的遗传结构对环境具有高度敏感性：在22个显著的数量性状位点（quantitative trait loci, QTL）中，仅1个在两种环境中被共同检测到。此外，我们还鉴定到在两种环境中均发挥作用的QTL，其等位基因对环境存在差异敏感性。综上，本研究结果表明，表型可塑性主要由特定环境下的特异性位点决定，但也可能受到跨环境作用位点的影响。最后，本研究的作图数据为重要调控位点ptch1通过遗传同化驱动可塑性演化提供了证据。整体而言，本研究解答了学界关于可塑性遗传基础与演化的长期争议，同时强调了环境在影响发育结局、遗传结构、形态多样性与进化潜力方面的关键作用。