Variation in limb loading magnitude and timing in tetrapods

Granatosky, M C and McElroy, E J and Lemelin, P and Reilly, S M and Nyakatura, J A and Andrada, E and Kilbourne, B M and Allen, V R and Butcher, M T and Blob, R W and Ross, C F (2019) Variation in limb loading magnitude and timing in tetrapods. JOURNAL OF EXPERIMENTAL BIOLOGY.

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Abstract

Comparative analyses of locomotion in tetrapods reveal two patterns of stride cycle variability. Tachymetabolic tetrapods (birds and mammals) have lower inter-cycle variation in stride duration than bradymetabolic tetrapods (amphibians, lizards, turtles, and crocodilians). This pattern has been linked to the fact that birds and mammals share enlarged cerebella, relatively enlarged and heavily myelinated Ia afferents, and γ-motoneurons to their muscle spindles. Tachymetabolic tetrapod lineages also both possess an encapsulated Golgi tendon morphology, thought to provide more spatially precise information on muscle tension. The functional consequence of this derived Golgi tendon morphology has never been tested. We hypothesized that one advantage of precise information on muscle tension would be lower and more predictable limb bone stresses, achieved in tachymetabolic tetrapods by having less variable substrate reaction forces than bradymetabolic tetrapods. To test this hypothesis, we analyzed hindlimb substrate reaction forces during locomotion of 55 tetrapod species in a phylogenetic comparative framework. Variation in species-means of limb loading magnitude and timing confirm that, for most of the variables analyzed, variance in hindlimb loading and timing is significantly lower in species with encapsulated versus unencapsulated Golgi tendon organs. These findings suggest that maintaining predictable limb loading provides a selective advantage for birds and mammals by allowing for energy-savings during locomotion, lower limb bone safety factors, and quicker recovery from perturbations. The importance of variation in other biomechanical variables in explaining these patterns, such as posture, effective mechanical advantage, and center-of-mass mechanics, remains to be clarified.