Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs
Pectoral and pelvic lobe-fins transformed into fore- and hindlimbs during the Devonian period, enabling the water-to-land transition in tetrapods. In the timespan of ~60 million years, transitional forms evolved, spanning a wide range of morphologies. Here we traced the evolution of well-articulated appendicular skeletons across the fins-to-limbs transition, using a network-based approach and phylogenetic tools to quantify and compare topological features of skeletal anatomy of fins and limbs. We show that the topological arrangement of bones in the pectoral and pelvic appendages evolved in parallel during the fins-to-limbs transition, occupying overlapping regions of the morphospace, following a directional mode of evolution, and decreasing their disparity over time. We identify the presence of digits as the morphological novelty triggering significant topological changes that clearly discriminated limbs from fins. The origin of digits caused an evolutionary shift towards appendages that were less densely and heterogeneously connected, but more assortative and modular. Topological disparity likewise decreased for both appendages: for the pectoral appendage, until the origin of amniotes; for the pelvic appendage, until a time concomitant with the earliest-known tetrapod tracks. Finally, we tested and rejected the presence of a pectoral-pelvic similarity bottleneck for the network-anatomy of appendages at the origin of tetrapods. We interpret our findings in the context of a dynamic compromise between possibly different functional demands in pectoral and pelvic appendages during the water-to-land transition and a shared developmental program constraining the evolvability of limbs.