A major paradigm shift in fish, tetrapod and limb evolution: characteristic tetrapod musculoskeletal limb phenotype emerged more than 400 MYA in basal lobe‐finned fishes

Abstract

Previous accounts of the origin of tetrapod limbs have postulated a relatively sudden change, after the split between extant lobe‐finned fish and tetrapods, from a very simple fin phenotype with only two muscles to the highly complex tetrapod condition. The evolutionary changes that led to the muscular anatomy of tetrapod limbs has therefore remained relatively unexplored. We performed dissections, histological sections, and MRI scans of the closest living relatives of tetrapods: coelacanths and lungfish. Combined with previous comparative, developmental and paleontological information, our findings suggest that the characteristic tetrapod musculoskeletal limb phenotype was already present in the Silurian last common ancestor of extant sarcopterygians, with exception to the autopod (hand/foot) structures, which have no clear correspondence with fish structures. Remarkably, the two major steps in this long process – leading to the ancestral fin anatomy of extant sarcopterygians and limb anatomy of extant tetrapods, respectively – occurred at the same nodes as the two major similarity bottlenecks that led to the striking derived myological similarity between the pectoral and pelvic appendages within each taxon. Our identification of probable homologies between appendicular muscles of sarcopterygian fish and tetrapods will allow more detailed reconstructions of muscle anatomy in early tetrapods.Support or Funding InformationAm. Assoc. Anat. postdoctoral grant to JLM, and European Union's Horizon 2020 Marie Skłodowska‐Curie grant No 654155 to BE‐A.