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 have 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 the exception of 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 and their relatives.

Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

“…Salamandra salamandra and Iguana iguana represent lissamphibians and squamates, respectively; differences from Ambystoma mexicanum and Sphenodon punctatus will be discussed. For this study we dissected specimens of S. punctatus, I. iguana, and S. salamandra, and we previously dissected specimens of N. forsteri, L. chalumnae, and A. mexicanum (Diogo et al, 2016) (Table 1).…”

“…Diogo et al (2016) included a new analysis of fin muscles in Latimeria based on dissections and computerized tomography (CT) scans (see also Miyake et al, 2016), and compared the resulting data with similar data from Neoceratodus and Ambystoma. The study proposed homology hypotheses based upon: (i) embryonic primordia and sequence of development [from Neoceratodus and Ambystoma (Boisvert et al, 2013); from Ambystoma (Diogo & Tanaka, 2014)]; (ii) comparative anatomy including architecture, innervation, topology, and attachments; and (iii) distribution of muscles within the phylogeny of each group (see Diogo et al, 2016, for detailed methods).…”

“…2A), and the insertion of the homologous muscle in Latimeria (a portion of the abductor superficialis; Diogo et al, 2016) is the ventral process of the humerus ('crochet du bord inferior' sensu Millot & Anthony, 1958) (Fig. 2B).…”

“…Their observations and comparisons indicated that many appendicular muscles present in extant dipnoans and coelacanths are homologous with muscles or muscle groups in tetrapods. Here, we re-examined the fossil literature in light of the new information and homology hypotheses provided by Diogo et al (2016) in order to reconstruct pectoral appendicular muscle anatomy in ancestral sarcopterygian fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods via EPB. First, we compiled records of osteological correlates of muscle attachment in sarcopterygian fish, including extant lungfish and coelacanths, and tetrapods, including extant lizards and salamanders, as well as various groups of extinct sarcopterygian fish and tetrapods, both from the literature and through direct examination of specimens.…”

“…Hutchinson, 2001). Diogo et al (2016) recently re-examined the muscle anatomy of the lungfish Neoceratodus (one of the only three extant genera of dipnoans) and the coelacanth Latimeria (the only extant coelacanth genus) and undertook a detailed comparison with other living fishes and with tetrapods in order to investigate the homology of appendicular muscles across these taxa. Their observations and comparisons indicated that many appendicular muscles present in extant dipnoans and coelacanths are homologous with muscles or muscle groups in tetrapods.…”