Coming to grips with life upside down: how myosin fiber type and metabolic properties of sloth hindlimb muscles contribu

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ORIGINAL PAPER

Coming to grips with life upside down: how myosin fiber type and metabolic properties of sloth hindlimb muscles contribute to suspensory function Kyle B. Spainhower1 · Allan K. Metz1 · Abdel‑Ruhman S. Yusuf1 · Lydia E. Johnson1 · Judy A. Avey‑Arroyo2 · Michael T. Butcher1  Received: 24 June 2019 / Revised: 15 September 2020 / Accepted: 28 October 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Sloths exhibit almost obligatory suspensory locomotion and posture. These behaviors require both strength and fatigue resistance, although we previously found muscle fiber type characteristics in the forelimbs of sloths that belied these initial expectations. Based on locomotor roles of the forelimbs versus hindlimbs in propulsion and braking, respectively, sloth hindlimb musculature should be adapted for force production and energy savings by a near homogeneous expression of slow myosin heavy chain (MHC) fibers. This hypothesis was tested by determining MHC fiber type (%) distribution and energy metabolism in the hindlimbs of three-toed (B. variegatus, N = 5) and two-toed (C. hoffmanni, N = 3) sloths. A primary expression of the slow MHC-1 isoform was found in the hindlimbs of both species. Slow MHC fiber type (%) was significantly greater in the flexors of B. variegatus, whereas expression of fast MHC-2A fibers was significantly greater in the extensors of C. hoffmannni. MHC-1 fibers were largest in cross-sectional area (CSA) and comprised the greatest %CSA in each muscle sampled from both species. Enzyme assays showed elevated activity for anaerobic enzymes (CK and LDH) compared with low-to-moderate activity for aerobic enzymes (3-HAD and CS), and only CK activity was related to body size. These findings emphasize a joint stabilization role by the hindlimbs during suspension, especially in smaller three-toed sloths, and suggest that larger two-toed sloths could have muscles further modified for greater power output and/or prolonged arboreal maneuvering. Moreover, modifications to muscle metabolism rather than MHC expression may be more reflective of functional adaptation in sloth limbs. Keywords  Arboreal · Metabolism · Muscle · Myosin heavy chain · Suspension Abbreviations 3-HAD 3-Hydroxyacetyl Co A dehydrogenase CK Creatine kinase CS Citrate synthase

CSA Cross-sectional area LDH Lactate dehydrogenase MHC Myosin heavy chain PFK Phosphofructokinase-1

Communicated by H.V. Carey.

Introduction

Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0036​0-020-01325​-x) contains supplementary material, which is available to authorized users. * Michael T. Butcher [email protected] 1



Department of Biological Sciences, Youngstown State University, 4013 Ward Beecher Science Hall, Youngstown, OH 44555, USA



The Sloth Sanctuary of Costa Rica, Penshurst, Limon, Costa Rica

2

Brown-throated three-toed (Bradypus variegatus) and Hoffmann’s two-toed (Choloepus hoffmanni) sloths are sympatric species throughout the neotropical rainfores