Variation in Articular Cartilage Thickness Among Extant Salamanders and Implications for Limb Function in Stem Tetrapods

Julia L Molnar

doi:10.3389/fevo.2021.671006

Abstract

The size and shape of articular cartilage in the limbs of extant vertebrates are highly variable, yet they are critical for understanding joint and limb function in an evolutionary context. For example, inferences about unpreserved articular cartilage in early tetrapods have implications for how limb length, joint range of motion, and muscle leverage changed over the tetrapod water-land transition. Extant salamanders, which are often used as functional models for early limbed vertebrates, have much thicker articular cartilage than most vertebrate groups, but the exact proportion of cartilage and how it varies across salamander species is unknown. I aimed to quantify this variation in a sample of 13 salamanders representing a broad range of sizes, modes of life, and genera. Using contrast-enhanced micro-CT, cartilage dimensions and bone length were measured non-destructively in the humerus, radius, ulna, femur, tibia, and fibula of each specimen. Cartilage correction factors were calculated as the combined thickness of the proximal and distal cartilages divided by the length of the bony shaft. Articular cartilage added about 30% to the length of the long bones on average. Cartilage was significantly thicker in aquatic salamanders (42 ± 14% in the humerus and 35 ± 8 in the femur) than in terrestrial salamanders (21 ± 7% in both humerus and femur). There was no consistent relationship between relative cartilage thickness and body size or phylogenetic relatedness. In addition to contributing to limb length, cartilage caps increased the width and breadth of the epiphyses by amounts that varied widely across taxa. To predict the effect of salamander-like cartilage correction factors on muscle leverage, a simplified model of the hindlimb of the Devonian stem tetrapodAcanthostegawas built. In this model, the lever arms of muscles that cross the hip at an oblique angle to the femur was increased by up to six centimeters. Future reconstructions of osteological range of motion and muscle leverage in stem tetrapods and stem amphibians can be made more rigorous by explicitly considering the possible effects of unpreserved cartilage and justifying assumptions based on available data from extant taxa, including aquatic and terrestrial salamanders.

Highlights

Articular cartilage morphology in extant taxa has been used as a basis to infer the extent of unpreserved cartilage in fossils animals for the purpose of reconstructing joint and limb function (e.g., Hutchinson et al, 2005; Jannel et al, 2019; Tsai et al, 2020; Molnar et al, 2021)
Ossification in the long bones of extant salamanders begins with a cartilaginous template, and bone is deposited around the periphery of the shaft, increasing the bone’s diameter (Francillon-Vieillot et al, 1990)
Articular cartilage was visible in both ends of each long bone and, in some specimens, at the tip of the greater trochanter of the femur (Figure 2)

Summary

Introduction

Articular cartilage morphology in extant taxa has been used as a basis to infer the extent of unpreserved cartilage in fossils animals for the purpose of reconstructing joint and limb function (e.g., Hutchinson et al, 2005; Jannel et al, 2019; Tsai et al, 2020; Molnar et al, 2021). In the case of stem tetrapods, salamanders may provide the most informative extant model for articular cartilage. The length of the bone is increased by periosteal bone deposited toward the epiphyses (Sanchez et al, 2010b) This epiphyseal cartilage hypertrophies and becomes calcified, and much of it is later resorbed to form the marrow cavity, which expands from the mid-shaft toward the epiphyses as the bone grows longer. Medullary trabecula following the same longitudinal pattern as the chondrocytes are formed by endochondral ossification (Haines, 1942)

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Results

Conclusion