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

Periodic Reporting for period 2 - LIMB NETWORKS (Network Analysis of Musculoskeletal Evolution and Modularity during the Fin-to-Limb Transition)

Reporting period: 2017-08-15 to 2018-08-14

"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, arm/thigh, forearm/leg and hand/foot. 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 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 divergence. New insights from comparative muscle anatomy in extant fishes and tetrapods indicate independently evolved similarities between the fore- and hindlimbs, which we sought to test.

Quantifying anatomical similarity between the fore- and hindlimbs requires improving the use of muscular data, as well as implementing new 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. 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 developed 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 were to gather musculoskeletal data from extant species, as well as to reconstruct muscle attachments in extinct species spanning the fin-limb transition, in order to build the first anatomical network models of limbs and of soft tissues such as muscles. We modelled anatomical networks using a multidisciplinary combination, for the first time, of (i) new data on fin/limb muscle anatomy in extant species, and (ii) reconstruction of muscle attachments in extinct forms (for which we provided preliminary insights that future studies can build upon). By combining muscular and skeletal data from extant and extinct species, together with the most advanced tools for the quantification of morphological modules, this project helps in resolving both i) the specific musculoskeletal details of the fin-limb transition, and ii) the fundamental and broader questions of how modularity facilitated morphological evolution across this transition in particular, and may influence macroevolution in general.

The importance to society is that we need to understand our ""inner fish""- how we came to be ourselves. Tetrapod limbs are critical aspects of our biology and they carry with them evolutionary ""baggage"" from our distant ancestors. We have the same bones: humerus, radius, ulna, etc. as in early fish and tetrapods; and joints connecting them. We also have many of the same muscles, connecting the bones in many of the same ways. Understanding how these evolved will impact our insight into how limbs function and develop today.

We found that the connections of bones in the fore- and hind- appendages evolved in parallel during the fins-to-limbs transition, following a directional rather than random mode of evolution, and decreasing their anatomical variation (""disparity"") over time. We identifed the presence of digits (fingers/toes) as the morphological novelty that discriminated limbs from fins. The origin of digits caused an evolutionary shift towards appendages that were more modular; i.e. more connected between each other than with other parts of the appendages. Thus digits were a novelty that facilitated morphological evolution. Finally, we tested and rejected the presence of a pectoral-pelvic similarity bottleneck for the skeletal connections of appendages at the origin of tetrapods; how bones connected to each other did not pass through phase of narrower variation at the fins-limbs transition. Overall, we found that how limbs were used in locomotion and how their development guided their form interacted in complex ways that limited the direction of their evolution across the fins-limbs transition."
We performed dissection of fins/limbs of eight extant species. Detailed descriptions of the anatomy of these species were published. Anatomical data were used to build the anatomical networks resulting in our first key article published in Evolution. We also studied the skeletal anatomy of the pectoral and pelvic appendages in 18 extinct genera. We used this anatomical information to build the anatomical networks of the fore- and hind- limbs/fins, and prepared an article that is currently under review in Science Advances; as a pre-print at Eight scientific articles directly stemmed from this project. We conducted further dissemination of this research via social media, and multiple conference presentations and workshops for professionals.
The development of empirical and theoretical computer models of musculoskeletal systems is a vanguard of current research in morphological sciences. This project combined 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 (progress was made here but not fully completed; regardless a strong foundation for future work was built). 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 pioneered in addressing the effects of morphological modularity on the evolutionary transition from fins to limbs. The quantitative analysis of morphological evolution provided by the research project was crucial to clarify the patterns of soft-hard tissue relationships in tetrapod limbs and therefore to provide a basis for more mechanistic developmental studies. There is no socio-economical impact or societal implications except the improved understanding of fundamental principles within evolution.