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Network Analysis of Musculoskeletal Evolution and Modularity during the Fin-to-Limb Transition

Periodic Reporting for period 1 - LIMB NETWORKS (Network Analysis of Musculoskeletal Evolution and Modularity during the Fin-to-Limb Transition)

Reporting period: 2015-08-15 to 2017-08-14

The fin-limb transition in vertebrates during the Late Devonian (~385mya) brought about the greatest morphological modifications of limbs, including the gradual differentiation of the forelimbs and hindlimbs. A central question in vertebrate evolution is how the various anatomical parts of fins evolved semi-autonomously (modularity) while still growing and adapting in coordination (integration) to a terrestrial function as limbs. According to anatomical and developmental criteria, the limbs of tetrapods are sub-divided into morphological modules such as the girdle, the stylopod (arm/thigh), the zeugopod (forearm/leg) and the autopod (hand/food). Although the fore- and hindlimb share a common developmental-genetic toolkit, their modular organization facilitates their semi-independent evolutionary change without impeding their coordinated function. During the fin-limb transition, the originally similar pelvic and pectoral fins of sarcopterygians evolved to fulfill different functions in land. Traditional studies on the evolution of limbs, mostly rooted in the comparative anatomy of hard tissues, have revealed an enduring anatomical similarity between the fore- and hindlimb after millions of years of evolutionary divergence. This similarity has supported the hypothesis of “serial homology”, which states that limbs are repetitive body elements with a common evolutionary origin that arose due to duplication and co-option of developmental mechanisms. Current advances in comparative myology, embryology, and paleobiology have however raised serious doubts about the validity of a true original serial homology to explain anatomical similarities between the fore- and hindlimbs. New insights from comparative muscle anatomy in extant fishes and tetrapods suggest that phylogenetically independent evolutionary changes, rather than serial homology, have lead to parallelisms and convergences– and, thus, to derived similarities–between the fore- and hindlimbs. As the first tetrapods adapted to terrestrial environments, the fore- and hindlimbs evolved different morphological adaptations to locomotion on land. Developmental studies suggest that the evolution of new muscles created topological asymmetries in the anatomy of the fore- and hindlimbs, whereas palaeobiological studies of hard tissues indicate that the fore- and hindlimbs performed different functions already in Devonian tetrapods. Coordinated morphological responses between the fore- and hindlimbs are necessary for adaptation; however, broader comparisons using bones and muscles often indicate that they can respond differentially in time and magnitude.

Quantifying anatomical similarity between the fore- and hindlimbs require improving the currently limited use of muscular data, as well as implementing innovative methods to compare modularity and integration among topologically disparate forms. Anatomical network models have been recently proposed to fill this methodological gap, by analyzing the topological pattern among anatomical parts like bones. This new approach quantifies structural properties such as modularity and integration by analyzing network models, in which nodes represent anatomical structures such as bones, and links represent physical contacts among them (e.g. joints or sutures). Using network models, anatomical similarity can be quantified and compared in the equivalence of connectivity modules and the strength of integration among modules. This project aims to develop an anatomical network analyses of muscles and of limbs to provide a comprehensive musculoskeletal study of the fin-limb transition, and specifically to unravel (i) the evolutionary changes in modularity of the musculoskeletal anatomy that occurred during this transition and (ii) how these newly acquired modular organizations might have facilitated the evolution of different morphologies for the fore- and hindlimbs in modern tetrapods.

The objectives of this project are to gather musculoskeleta
We have performed dissection of limbs of Ambystoma mexicanum, and Salamandra salamandra; we also gathered the information of Neoceratodus forsteri and Latimeria chalumnae from computed tomography scans. These are species included in the project proposal. Additionally, we are completing the sample of species with dissections of Polypterus senegalus, Sphenodon punctatus, Rattus norvegicus, and Didelphis virginiana, for comparison.

The detailed descriptions of the anatomy of the fins and limbs in these species have been published or are under review. Anatomical information has been used to build the anatomical networks of the fore- and hind- limbs/fins, and the first article presenting the results has been submitted for publication.

Additionally, we have published an methodological article describing the new techniques implemented in this project, and systematic review on the broader problematic of studying morphological modularity in complex living beings. Both publications appeared in prestigious peer-review journal.
The development of empirical and theoretical computer models of musculoskeletal systems is a vanguard of current research in morphological sciences. This project combines three complementary cutting-edge approaches: (i) reconstruction of the musculoskeletal anatomy of extinct species, (ii) anatomical networks modeling of limbs, and (iii) including not only bones but also muscles in these networks. Most studies on morphological evolution in the last decades have focused on skeletal structures; only a few research groups have focused mainly on muscles, and even fewer have focused on the relationships between hard and soft tissues. Moreover, most studies on limb evolution consider only the analysis of hard tissues, whereas muscular data have been mostly used in biomechanical locomotor models. This project is pioneering in addressing the effects of morphological modularity on the evolutionary transition from fins to limbs. The quantitative analysis of morphological evolution that will be provided by the proposed research project is crucial to clarify the patterns of soft-hard tissue relationships in tetrapod limbs and therefore to provide a basis for more mechanistic developmental studies.
Visual abstract of the objectives for the first part of the project