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.

Mechanosensation is fundamental to many tetrapod limb functions yet it remains largely uninvestigated in the paired fins of fishes, the limb homologs. Here we examine whether membranous fins may function as passive structures for touch sensation in the absence of extensive fin ray movement. We investigate the pectoral fins of the pictus catfish (Pimelodus pictus), a species that lives in close association with the benthic substrate and whose fins are positioned near its ventral margin. Kinematic analysis shows that the pectoral fins are held at a constant angle of partial protraction during routine forward swimming and do not appear to generate propulsive force. Immunohistochemistry reveals that the fins are highly innervated and we observe putative mechanoreceptors at nerve fibre endings. To test for the ability to sense mechanical perturbations, activity of fin ray nerve fibres was recorded in response to touch and bend stimulation. Both pressure and light surface brushing generated afferent nerve activity. Fin ray nerves also respond to bending of the rays. These data demonstrate for the first time that membranous fins can function as passive mechanosensors and suggest that touch sensitive fins may be widespread in fishes that maintain a close association with the bottom substrate.