Network architecture associated with the highly specialized hindlimb of frogs

Abstract

Network analyses have been increasingly used in the context of comparative vertebrate morphology. The structural units of the vertebrate body are treated as discrete elements (nodes) of a network, whose interactions at their physical contacts (links) determine the phenotypic modules. Here, we use the network approach to study the organization of the locomotor system underlying the hindlimb of frogs. Nodes correspond to fibrous knots, skeletal and muscular units. Edges encode the ligamentous and monoaxial tendinous connections in addition to joints. Our main hypotheses are that: (1) the higher centrality scores (measured as betweenness) are recorded for fibrous elements belonging to the connective system, (2) the organization of the musculoskeletal network belongs to a non-trivial modular architecture and (3) the modules in the hindlimb reflect functional and/or developmental constraints. We confirm all our hypotheses except for the first one, since bones overpass the fibrous knots in terms of centrality. Functionally, there is a correlation between the proximal-to-distal succession of modules and the progressive recruitment of elements involved with the motion of joints during jumping. From a developmental perspective, there is a correspondence between the order of the betweenness scores and the ontogenetic chronology of hindlimbs in tetrapods. Modular architecture seems to be a successful organization, providing of the building blocks on which evolution forges the many different functional specializations that organisms exploit.

Phylogenetic patterns and correlation of key structures for jumping: bone crests and cross‐sectional areas of muscles inLeptodactylus(Anura, Leptodactylidae)

“…All these characters contribute to the development and functionality of the hip module (Dos Santos et al. ), whose integrated skeletal, muscular and tendinous elements are closely tied to functional variations.…”

“…sagittal-hinge, lateral-bender), urostylar fusion or bicondyly, and the ilium length that is key to the pelvic glide (Emerson, 1979(Emerson, , 1982Reilly & Jorgensen, 2011;Jorgensen & Reilly, 2013;Herrel et al 2014). All these characters contribute to the development and functionality of the hip module (Dos Santos et al 2017), whose integrated skeletal, muscular and tendinous elements are closely tied to functional variations.…”

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

“…Here, we formalized the anatomical organization of fins and limbs using network models that capture the basic physical relationships among bones and muscles. Working with network models of the musculoskeletal anatomy of appendages allows us to directly compare forms with incomplete homologies , to integrate skeletal and muscular data 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).…”

Comparative anatomy and development of pectoral and pelvic girdles in hylid anurans

“…Based on a matrix primarily composed of developmental data, we optimized the characters on the most recent published phylogeny for hylids (Duellman, Marion, & Hedges, 2016) to identify evolutionary trends of girdle structure in the family. Comparative studies of girdles are particularly relevant to elucidate serial homologies in their structure (Diogo & Molnar, 2014;Diogo & Tanaka, 2014;Diogo & Ziermann, 2014Diogo, Linde-Medina, Abdala, & Ashley-Ross, 2013;Sears et al, 2015), especially given that the ontogeny of the proximal limb segments is closely associated with the development of the girdles (Dos Santos, Fratani, Ponssa, & Abdala, 2017;Manzano et al, 2013;Pomikal & Streicher, 2010;Pomikal et al, 2011). Additionally, our understanding of the development of anuran girdles is limited in contrast to our understanding of limb development.…”