Data from: Mechanosensation is evolutionarily tuned to locomotor mechanics

The biomechanics of animal limbs has evolved to meet the functional demands for movement associated with different behaviors and environments. Effective movement relies not only on limb mechanics but also on appropriate mechanosensory feedback. By comparing sensory ability and mechanics within a phylogenetic framework, we show that peripheral mechanosensation has evolved with limb biomechanics, evolutionarily tuning the neuromechanical system to its functional demands. We examined sensory physiology and mechanics of the pectoral fins, forelimb homologs, in the fish family Labridae. Labrid fishes exhibit extraordinary morphological and behavioral diversity and employ pectoral fin-based propulsion with fins ranging in shape from high aspect ratio (AR) wing-like fins to low AR paddle-like fins. Phylogenetic character analysis demonstrates that high AR fins evolved independently multiple times in this group. Four pairs of species were examined; each included a pleseiomorphic low AR and a high AR species. Within each species pair, the high AR species demonstrated significantly stiffer fin rays in comparison to the low AR species. Afferent sensory nerve activity was recorded during fin ray bending. In all cases, afferents of stiffer fins were more sensitive at lower displacement amplitudes demonstrating mechanosensory tuning to fin mechanics, and a consistent pattern of correlated evolution. We suggest that this is a clear example of parallel evolution in a complex neuromechanical system, with a strong link between multiple phenotypic characters: pectoral fin shape, swimming behavior, fin ray stiffness, and mechanosensory sensitivity.

动物肢体的生物力学演化，旨在适配不同行为与环境对应的运动功能需求。高效运动不仅依赖肢体自身的力学特性，同时也离不开恰当的机械感觉反馈。本研究通过在系统发育框架内比较感觉能力与力学特征，发现外周机械感觉系统会随肢体生物力学共同演化，进而将神经力学系统优化至匹配其功能需求的状态。我们以隆头鱼科（Labridae）鱼类的胸鳍——前肢同源器官——为研究对象，分析了其感觉生理学与力学特性。隆头鱼科鱼类具有极强的形态与行为多样性，其推进方式依赖胸鳍，鳍的形态跨度极大，从高展弦比（aspect ratio, AR）翼状鳍延伸至低展弦比桨状鳍。系统发育性状分析表明，高展弦比鳍在该类群中独立演化了多次。本次研究共分析了四组物种对，每组均包含1个祖征性低展弦比物种与1个高展弦比物种。在每组物种对中，高展弦比物种的鳍条刚度显著高于低展弦比物种。我们在鳍条弯曲过程中记录了传入感觉神经的电活动，结果显示，所有测试组中高刚度鳍的传入神经对更低位移振幅的刺激更为敏感，这表明机械感觉系统会根据鳍的力学特性进行适配调整，且二者存在协同演化的一致模式。我们认为，该研究清晰展现了复杂神经力学系统中的平行演化现象，且胸鳍形态、游泳行为、鳍条刚度与机械感觉敏感性这多个表型性状之间存在紧密关联。