Abstract
One of the most intriguing questions in vertebrate evolution is how tetrapods gained the ability to walk on land. Although many hypotheses have been proposed, few have been rigorously tested using the fossil record. Here, we build three-dimensional musculoskeletal models of the pectoral appendage in Eusthenopteron, Acanthostega, and Pederpes and quantitatively examine changes in forelimb function across the fin-to-limb transition. Through comparison with extant fishes and tetrapods, we show that early tetrapods share a suite of characters including restricted mobility in humerus long-axis rotation, increased muscular leverage for humeral retraction, but not depression/adduction, and increased mobility in elbow flexion-extension. We infer that the earliest steps in tetrapod forelimb evolution were related to limb-substrate interactions, whereas specializations for weight support appeared later. Together, these results suggest that competing selective pressures for aquatic and terrestrial environments produced a unique, ancestral "early tetrapod" forelimb locomotor mode unlike that of any extant animal.
Highlights
The evolution of terrestrially capable tetrapod limbs from aquatically adapted fins has inspired decades of scientific investigation
Our results show a combination of maximum osteological range of motion (ROM) and muscle leverage in the forelimb of early tetrapods that is distinct from that of both extant finned sarcopterygians and modern tetrapods, leading us to infer a unique form of locomotor specialization for living at the interface between water and land
The first is from a “benthic fish ancestor” locomotor mode resembling extant lungfish to an “early tetrapod” mode that has no close extant analog
Summary
The evolution of terrestrially capable tetrapod limbs from aquatically adapted fins has inspired decades of scientific investigation. Multiple locomotor hypotheses have been proposed on the basis of analysis of the early tetrapod fossil record, ranging from underwater walking to fully terrestrial quadrupedal gaits and various modes in between [10]. Muscle leverage (quantified by moment arms) influences the maximum rotational force and velocity of movements of a joint, or the ability to stabilize a joint against motion [e.g., [30]] Together, these metrics can reveal trade-offs in the locomotor system such as stability versus mobility and limb forces versus arcs of movement, allowing us to test functional hypotheses in extinct animals. Our results show a combination of maximum osteological ROM and muscle leverage in the forelimb of early tetrapods that is distinct from that of both extant finned sarcopterygians and modern tetrapods, leading us to infer a unique form of locomotor specialization for living at the interface between water and land
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