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.

Keywords: Labridae; evolution; locomotion; mechanosensation; neuromechanics.

Fig. S1.

A comparison of pectoral fin ray bending during a typical fin stroke between two closely related species using different aspect ratio fins. (A) The pectoral fins of the low aspect ratio rower, H. bivittatus, undergo considerable bending throughout their fin stroke, (B) whereas the pectoral fins of the high aspect ratio flapper, G. varius, remain relatively straight through their fin stroke. In A, Right and B, Right, the pectoral fin is highlighted. The interspecific differences in fin bending magnitude are highlighted in C, and, again, after being normalized to the same length, in D.

Fig. 1.

The phylogenetic relationships of the Labridae and pectoral fin aspect ratio ancestral state reconstruction. The maximum likelihood reconstruction revealed a most likely ancestral state of low aspect ratio pectoral fins (low = 0.47, intermediate = 0.29, high = 0.24) and at least 22 independent evolutions of high aspect ratio fins. An arrow and the species’ initials highlights the phylogenetic position of each species used in this study. The two species of each pair were always located within the same subfamily and each species pair contains an independent evolution of the high AR fin. The phylogeny presented here is pruned from 340 species to 150 species to maximize visualization. The ancestral state of the basal node is taken from the 340 species reconstruction. The full 340 species phylogeny and accompanying 340 species ancestral state reconstruction can be found in Fig. S2, and the node labels and the corresponding likelihood of the ancestral state at each node can be found in Fig. S3 and Table S1, respectively. Red, high aspect ratio; yellow, intermediate aspect ratio; and blue, low aspect ratio. Photo credits: H. bivittatus, Paul Humann; H. hortulanus and G. varius, Jeffrey T. Williams; and B. rufus, C. parrae, C. fasciatus, H. melanurus, and S. taeniopterus, John E. Randall.

Fig. S2.

The phylogenetic relationships and pectoral fin aspect ratio ancestral state reconstruction of 340 species within the family Labridae. The maximum likelihood reconstruction revealed a most likely ancestral state of low aspect ratio pectoral fins or the rowing swimming behavior (low = 0.47, intermediate = 0.29, high = 0.24) and at least 22 independent evolutions of high aspect ratio fins (or the flapping swimming behavior). The node labels and the corresponding likelihood of the ancestral state at each node can be found in Fig. S2 and Table S1, respectively. Red, high aspect ratio; yellow, intermediate aspect ratio; and blue, low aspect ratio.

Fig. S3.

The 340 species Labridae phylogeny with all nodes labeled. The corresponding likelihood of the ancestral state at each node can be found in Table S1. The labels for nodes closest to the tip are shown next to the corresponding tips.

Fig. 2.

Comparative pectoral fin morphology, mechanics, and proprioceptive sensitivity between closely related low AR (C. fasciatus) and high AR (S. taeniopterus) species. (A) Cleared and stained pectoral fins of S. taeniopterus (flapper; Top) and C. fasciatus (rower; Bottom). S. taeniopterus employs wing-like high-aspect ratio pectoral fins, whereas C. fasciatus employs broad paddle-like pectoral fins. (Scale bars, 1 cm.) (B) The pectoral fin rays of S. taeniopterus (high AR; red) are significantly stiffer than the rays of C. fasciatus (low AR; blue). All flexural stiffness data for each species were pooled and fit with an exponential curve (r² = 0.93, 0.95 for S. taeniopterus and C. fasciatus, respectively). Correspondingly, the data are presented in a semilog fashion with a logarithmically scaled y axis. The shaded region of each fit represents a 99% confidence interval of the linear regression. The y intercept and slope of the regression line was significantly different between each species (P < 0.05; Table S2). (C) Representative nerve recordings from one individual of S. taeniopterus (Left) and C. fasciatus (Right). A three times larger bending magnitude is needed to elicit a response in the size-matched pectoral fin of the flexible-finned C. fasciatus in comparison with the stiff-finned S. taeniopterus.

Fig. S4.

A comparison of pectoral fin ray flexural stiffness among the individuals of each species. In all cases, the pectoral fin rays of flappers are significantly stiffer than those of rowers. Exponential curves were fit using least squares to the pooled data for each species. The shaded regions represent the 99% confidence interval around the exponential fit. There is never an overlap of the confidence interval between two species of the same pair. Regression statistics are detailed in Table S1.

Fig. 3.

Summary of afferent response to fin ray bending. (A) Bivariate plots of burst duration by fin ray bending magnitude per species. The duration of bursts (three or more spikes within 50 ms of each other) associated with the onset of fin ray movement is positively and significantly correlated with fin ray bending magnitude. Regression lines are presented for one representative individual of each species, and regression statistics for all individuals are detailed in Table S3. Arrows represent minimum response amplitude per species. (B) Response threshold (the minimum bending amplitude needed to elicit a response) is plotted against fin ray flexural stiffness for every individual of each species. In all cases, the pectoral fin rays of high AR fins are significantly stiffer than those of low AR fins, and the proprioceptive system of high AR species is significantly more sensitive than that of low AR species. Blue, flexible low AR fins; red, stiff high AR fins.

Fig. S5.

Summary of afferent response to fin ray bending during the hold period of step-and-hold stimuli. Bivariate plots of hold period spike rate by fin ray bending magnitude per species are shown. Hold period spike rate is positively and significantly correlated with fin ray bending magnitude. Regression lines are presented for one representative individual of each species, and regression statistics for all individuals are detailed in Table S5.