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) 可使生物随环境变化改变自身表型。尽管其是当前演化潜力研究领域的核心议题之一，但对于正在经历适应性分化的类群，学界仍缺乏对其可塑性遗传基础的全面认知。本研究以经典教材中收录的适应性辐射 (adaptive radiation) 类群——马拉维湖丽鱼科鱼类为研究对象，探究其表型可塑性的遗传基础。
具体而言，本研究通过杂交两个分化程度迥异的物种，构建了F3代杂交定位群体。在幼体早期阶段，研究团队将杂交家系分为两组，分别饲养于两种模拟自然觅食模式的环境中：其一为底栖刮食环境，其二为浮游抽吸环境。两种处理诱导产生的形态变异，与马拉维湖丽鱼的主要分化轴高度吻合，为适应性辐射的灵活茎理论 (flexible stem theory) 提供了实验支撑。
进一步研究发现，多个形态性状的遗传架构 (genetic architecture) 对环境具有高度敏感性。具体来说，在22个具有显著效应的数量性状基因座 (quantitative trait loci, QTL) 中，仅1个在两种环境中均被检测到。此外，本研究还鉴定到一类在两种环境中均发挥功能的QTL，其不同等位基因对环境的响应存在显著差异。据此，本研究结果表明：表型可塑性主要由特定环境下特异性表达的基因座决定，但也可能受到跨环境发挥作用的基因座的调控。
最后，本研究的定位数据为关键调控基因座ptch1通过遗传同化 (genetic assimilation) 演化出可塑性提供了直接实验证据。综上，本研究解答了学界长期以来关于表型可塑性遗传基础与演化的诸多争议，同时也凸显了环境在调控发育结局、遗传架构、形态多样性及演化潜力等方面的核心作用。