Data from: Many-to-one form-to-function mapping weakens parallel morphological evolution

Evolutionary ecologists aim to explain and predict evolutionary change under different selective regimes. Theory suggests that such evolutionary prediction should be more difficult for biomechanical systems in which different trait combinations generate the same functional output: “many-to-one mapping”. Many-to-one mapping of phenotype to function enables multiple morphological solutions to meet the same adaptive challenges. Therefore, many-to-one mapping should undermine parallel morphological evolution, and hence evolutionary predictability, even when selection pressures are shared among populations. Studying 16 replicate pairs of lake- and stream-adapted threespine stickleback (Gasterosteus aculeatus), we quantified three parts of the teleost feeding apparatus and used biomechanical models to calculate their expected functional outputs. The three feeding structures differed in their form-to-function relationship from one-to-one (lower jaw lever ratio) to increasingly many-to-one (buccal suction index, opercular 4-bar linkage). We tested for (1) weaker linear correlations between phenotype and calculated function, and (2) less parallel evolution across lake-stream pairs, in the many-to-one systems relative to the one-to-one system. We confirm both predictions, thus supporting the theoretical expectation that increasing many-to-one mapping undermines parallel evolution. Therefore, sole consideration of morphological variation within and among populations might not serve as a proxy for functional variation when multiple adaptive trait combinations exist.进化生态学家旨在阐释并预测不同选择模式下的进化变化。理论指出，对于存在不同性状组合可产生相同功能输出的生物力学系统，这类进化预测的难度更高——这类机制被称为多对一映射（many-to-one mapping）。表型（phenotype）到功能的多对一映射，使得生物可通过多种形态学解决方案应对相同的适应性挑战。因此，即便不同种群共享相同的选择压力，多对一映射仍会削弱平行形态进化（parallel morphological evolution），进而降低进化可预测性。本研究以16组重复的湖泊适应性与溪流适应性三棘刺鱼（Gasterosteus aculeatus）配对样本为研究对象，量化了硬骨鱼（teleost）摄食器官的三个组成部分，并借助生物力学模型计算其预期功能输出。这三种摄食结构的形态-功能关系各不相同：从严格的一对一关系（下颌杠杆比），到逐渐增强的多对一映射关系（口腔吸力指数、鳃盖四杆连杆机构）。我们针对两项预测开展了检验：（1）相较于一对一映射系统，多对一映射系统中表型与计算所得功能之间的线性相关性更弱；（2）跨湖-溪种群配对的平行进化程度更低。本研究证实了这两项预测，从而支持了“多对一映射程度越高，平行进化程度越低”的理论预期。因此，当存在多种适应性性状组合时，仅考虑种群内部及种群间的形态学变异，或许无法作为功能变异的替代指标。