Anatomical network analysis of the musculoskeletal system reveals integration loss and parcellation boost during the fins-to-limbs transition

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.

Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs

“…At the same time, phalanges articulating one-on-one proximodistally increased the overall path length (L) of appendages and the assortativity of bones (A). Last, the formation of new digit modules increased the parcellation (P) of limbs compared to lobe-fins, making them more modular ( 23 ). The origin of digits was concomitant with the parallel evolution of pectoral and pelvic limbs toward a region of the morphospace (Fig.…”

“…1A). This level of abstraction allowed us to compare evolutionary changes that are not amenable to quantification using other morphometric methods due to the large disparity of forms and presence/absence of parts between pectoral and pelvic fins and limbs ( 23 , 27 , 28 ). Furthermore, the abstraction retains biological meaning in that the contacts between skeletal elements reflect potential direct developmental and biomechanical interactions, for example, ontogenetic sequences of ossification or embryonic interaction, and joint reaction forces or ranges of motion.…”

“…Furthermore, the abstraction retains biological meaning in that the contacts between skeletal elements reflect potential direct developmental and biomechanical interactions, for example, ontogenetic sequences of ossification or embryonic interaction, and joint reaction forces or ranges of motion. Using a network-based approach ( 23 , 29 , 30 ), we modeled the skeleton of fully articulated appendages as networks, in which nodes code for bones and links code for physical contact in a standardized resting pose. We compared the evolution of eight network-based topological variables (see Methods for details) in a phylogenetic context (Fig.…”

Birds have peramorphic skulls, too: anatomical network analyses reveal oppositional heterochronies in avian skull evolution

“…In addition, we also calculated the parcellation (P), which measures the extent to which the nodes of a network are divided into balanced modules. The theoretical background of these module analyses are described, among others, in Werneburg et al 11 , Rasskin-Gutman and Esteve-Altava 51 , Esteve-Altava et al 52,56 and Clauset et al 55 .…”

A node-based informed modularity strategy to identify organizational modules in anatomical networks

“…articulations), and then quantifies their topological organization as a proxy to understand the biological features of the organism. Anatomical studies using network analysis have focused on comparing the development, function, and evolution of morphological systems, from invertebrates to vertebrates, including extant and extinct organisms ( Dos Santos et al, 2017 ; Esteve-Altava et al, 2013a , b , 2018 , 2019 ; Fernández et al, 2020 ; Fontanarrosa et al, 2020 ; Kerkman et al, 2018 ; Murphy et al, 2018 ; Ostachuk, 2019 ; Plateau and Foth, 2020 ; Saucède et al, 2015 ; Sookias et al, 2020 ).…”