Evolution of Hindlimb Muscle Anatomy Across the Tetrapod Water-to-Land Transition, Including Comparisons With Forelimb Anatomy.

Julia L Molnar,John R Hutchinson,Rui Diogo,Stephanie E Pierce

doi:10.1002/ar.23997

Abstract

Tetrapod limbs are a key innovation implicated in the evolutionary success of the clade. Although musculoskeletal evolution of the pectoral appendage across the fins-to-limbs transition is fairly well documented, that of the pelvic appendage is much less so. The skeletal elements of the pelvic appendage in some tetrapodomorph fish and the earliest tetrapods are relatively smaller and/or qualitatively less similar to those of crown tetrapods than those of the pectoral appendage. However, comparative and developmental works have suggested that the musculature of the tetrapod forelimb and hindlimb was initially very similar, constituting a "similarity bottleneck" at the fins-to-limbs transition. Here, we used extant phylogenetic bracketing and phylogenetic character optimization to reconstruct pelvic appendicular muscle anatomy in several key taxa spanning the fins-to-limbs and water-to-land transitions. Our results support the hypothesis that transformation of the pelvic appendages from fin-like to limb-like lagged behind that of the pectoral appendages. Compared to similar reconstructions of the pectoral appendages, the pelvic appendages of the earliest tetrapods had fewer muscles, particularly in the distal limb (shank). In addition, our results suggest that the first tetrapods had a greater number of muscle-muscle topological correspondences between the pectoral and pelvic appendages than tetrapodomorph fish had. However, ancestral crown-group tetrapods appear to have had an even greater number of similar muscles (both in terms of number and as a percentage of the total number of muscles), indicating that the main topological similarity bottleneck between the paired appendages may have occurred at the origin of the tetrapod crown group. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:218-234, 2020. © 2018 American Association for Anatomy.

Highlights

The origin of tetrapod limbs from fish fins was not a series of stepwise changes from fishlike to tetrapod-like morphology
At node 6, distinct groups of scars appeared on the lateral aspect of the ilium just above the acetabulum marking the origins of extensor iliotibialis and tenuissimus; scars appeared on the fibular epicondyle marking the origin of extensor cruris et tarsi fibularis; a distinct scar appeared on the dorsal aspect of the femoral head, marking the insertion of ischiotrochantericus; and the ventral ridge of the tibia appeared, marking the origins of extensor cruris tibialis and extensor tarsi tibialis
Comparisons with previous studies Several previous studies have attempted to reconstruct appendicular muscle anatomy in early tetrapods and their relatives, most have focused on the pectoral appendage (Romer 1924; Miner 1925; Andrews and Westoll 1970; Holmes 1977; e.g., Ahlberg 1989; Bishop 2014; Molnar et al 2017a)

Summary

Introduction

The origin of tetrapod limbs from fish fins was not a series of stepwise changes from fishlike to tetrapod-like morphology. The earliest known tetrapod hindlimbs (belonging to the Devonian tetrapods Ichthyostega and Acanthostega) had more than five digits (Coates and Clack 1990). Ichthyostega had a unique combination of postcranial characteristics: a derived forelimb with an anteroventrally positioned radial articulation and a bifid olecranon process, a paddle-like hindlimb, and a vertebral column with an almost mammal-like degree of regionalization (Ahlberg et al 2005; Pierce et al 2012, 2013a, b). The balance of evidence from fossil, evo-devo, and functional studies suggests that the transformation of the pelvic appendage lagged behind that of the pectoral appendage (Andrews and Westoll 1970; Edwards 1977; Boisvert 2005; Cole et al 2011; Pierce et al 2013b; Shubin et al 2014). Several studies have suggested divergent functions for the forelimb and the hindlimb during locomotion (e.g., Gregory 1928; Ahlberg et al 2005; Boisvert 2005; Pierce et al 2012, 2013b)

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Results

Discussion

Conclusion