Abstract

Tetrapods evolved from within the lobe-finned fishes around 370 Ma. The evolution of limbs from lobe-fins entailed a major reorganization of the skeletal and muscular anatomy of appendages in early tetrapods. Concurrently, a degree of similarity between pectoral and pelvic appendages also evolved. Here, we compared the anatomy of appendages in extant lobe-finned fishes (Latimeria and Neoceratodus) and anatomically plesiomorphic amphibians (Ambystoma, Salamandra) and amniotes (Sphenodon) to trace and reconstruct the musculoskeletal changes that took place during the fins-to-limbs transition. We quantified the anatomy of appendages using network analysis. First, we built network models-in which nodes represent bones and muscles, and links represent their anatomical connections-and then we measured network parameters related to their anatomical integration, heterogeneity, and modularity. Our results reveal an evolutionary transition toward less integrated, more modular appendages. We interpret this transition as a diversification of muscle functions in tetrapods compared to lobe-finned fishes. Limbs and lobe-fins show also a greater similarity between their pectoral and pelvic appendages than ray-fins do. These findings on extant species provide a basis for future quantitative and comprehensive reconstructions of the anatomy of limbs in early tetrapod fossils, and a way to better understand the fins-to-limbs transition.

Highlights

  • The limbs of tetrapods evolved from the lobe-fins of sarcopterygian fishes around 370 Ma through a series of anatomical innovations (Fig. 1A)

  • We studied the pectoral and pelvic appendages in five extant taxa that phylogenetically bracket the fins-to-limbs transition: two lobefinned fishes, the African coelacanth Latimeria chalumnae and the Australian lungfish Neoceratodus forsteri; and three tetrapods, the axolotl Ambystoma mexicanum, the fire salamander Salamandra salamandra, and the tuatara Sphenodon punctatus

  • COMPARISON OF SKELETAL NETWORKS The skeletons of fore- and hind limbs of tetrapods (Fig. 4) have more elements (N) than the pectoral and pelvic ray-fins of Polypterus and lobe-fins of Latimeria, but fewer than the lobe-fins of Neoceratodus. This difference between Latimeria and Neoceratodus is due to the derived anatomy of Neoceratodus fins, which are composed of a long series of mesomeres, each one articulating with preaxial and postaxial radials

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Summary

Introduction

The limbs of tetrapods evolved from the lobe-fins of sarcopterygian fishes around 370 Ma through a series of anatomical innovations (Fig. 1A). The study of the origin of limbs involves working with uncertain homologies between anatomical structures, reconstructing soft tissue in transitional fossil taxa, and gathering information from the few extant taxa close to the fins-to-limbs transition (e.g., Molnar et al 2017). These circumstances present a challenge for quantitative methods comparing the anatomical organization of appendages, especially in very disparate forms. Compare forms with incomplete homologies (Diogo et al 2015), to integrate skeletal and muscular data (Diogo et al 2015; Molnar et al 2017; Santos et al 2017), and to quantify patterns of morphological complexity, integration, and modularity in a manner not available for comparative methods that focus on shape and size (Kerkman et al 2017; Esteve-Altava 2017a; Murphy et al 2018)

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