Mechanosensation is evolutionarily tuned to locomotor mechanics

Abstract

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 use 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 plesiomorphic low AR and a high AR species. Within each species pair, the high AR species demonstrated significantly stiffer fin rays in comparison with 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 these data provide 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.

The influence of size on body shape diversification across Indo‐Pacific shore fishes*

“…Another noteworthy clade-specific result includes our finding of both low disparity and low rates of body shape evolution in Labridae, a family with exceptionally high trophic diversity (Hiatt and Strasburg 1960;Randall 1967). Although other studies have revealed that this group shows tremendous variation in functional traits associated with feeding performance (Yamaoka 1978;Clifton and Motta 1998;Wainwright et al 2004) and locomotion (Wainwright et al 2002;Aiello et al 2017), this does not seem to translate into variation in body shape.…”

Understanding the origin of the most isolated endemic reef fish fauna of the Indo‐Pacific: Coral reef fishes of Rapa Nui

“…Species were placed in the phylogenies of cheilodactylids (Burridge & Smolenski, ), holocentrids (Dornburg et al., ), kuhliids (Feutry et al., ), monacanthids (Santini, Sorenson, & Alfaro, ), pomacanthids (Gaither et al., ) and pomancentrids (Frédérich, Sorenson, Santini, Slater, & Alfaro, ) while several phylogenies were used to compose the dataset of chaetodontids (Cowman and Bellwood () for eight of the nine genes and Gaboriau, Leprieur, Mouillot, and Hubert () for COI). For labrids, we used the 12S, 16S, Tmo‐4C4, RAG2, S7 and COI genes as described in Aiello, Westneat, and Hale () and followed the methodology of Wainwright et al. (): we included only a few representatives of all genuses other than that of the target species (Table ).…”

Variation in flexural stiffness of the lepidotrichia within and among the soft fins of yellow perch under different preservation techniques

“…Aiello et al () have also demonstrated that the stiffness of the rays decreased in individual fin rays in the proximo‐distal direction, and among fin rays along the chord of the fin moving from the leading to the trialing edge (). Another analysis of the mechanics of fins and fin rays (Aiello et al, ) demonstrated that there is a strong association between a fin's aspect ratio (length/width) and the material properties of its rays. Specifically, the rays of high aspect ratio pectoral fins, which are used primarily for lift‐based “flapping” propulsion, are much more stiff than those in species with low aspect‐ratio fins.…”

“…Muscle contraction at the base of the fin can generate forces that control the position of the rays relative to one another, as well as the curvature along the length of individual fin rays (Alben et al, ; Arita, ; Geerlink & Videler, ; Chadwell & Ashley‐Ross, ; Lauder, ). The fact that fin rays provide support and define fin function as a whole has led to a burgeoning interest in the relationship between fin ray morphology and fin performance (Aiello, Westneat, & Hale, ; Aiello et al, ; Alben et al, ; Chadwell & Ashley‐Ross, ; Chadwell et al, ; Flammang, Alben, Madden, & Lauder, ; Geerlink & Videler, ; Taft & Taft, ).…”