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.
