The dermal skeleton of stem-actinopterygian Moythomasia durgaringa and its implications for the nature of the ancestral osteichthyan

The dermal skeleton is the most primitive component of the vertebrate mineralized skeleton and features of its structure and development are key to resolving the evolutionary relationships of early vertebrates and bony fishes. In particular, the nature and phylogenetic distribution of cosmine, a dermal complex of hard tissue and vascular systems, has been the focus of debate over the nature of the ancestral osteichthyan and the timing of actinopterygian-sarcopterygian divergence. In large part, this controversy occurs because of a paucity of knowledge of the nature of the dermal skeleton in stem-actinopterygians. Here we describe the dermal skeletal histology of stem-actinopterygian Moythomasia durgaringa, using Scanning Electron Microscopy and Synchrotron Radiation X-ray Tomographic Microscopy with a reconstruction of its topological variation and development. The dermal skeleton of Moythomasia consists of a superficial layer of stacked odontodes that undergo extensive odontogenic resorption, and a basal layer of lamellar bone. A middle vascular bone layer is variably developed in cranial dermal bones but is completely absent in postcranial dermal elements. Additional histological variation among dermal elements includes the number of odontode generations, odontode growth patterns, and the relative thickness of osteogenic and odontogenic tissues. A comparison of the histological condition in Moythomasia and stem- and early crown-osteichthyans reveals numerous similarities, including the presence of a three-layered dermal skeleton, stacked odontodes, and odontogenic resorption. Phylogenetic comparative analyses on early jawed vertebrates indicate that features associated with cosmine evolved in groups outside Osteolepiformes, while true cosmine remains restricted to this group. The concept of cosmine is phylogenetically uninformative because of the multiplicity of its definitions and usage. These findings suggest that fossil taxa currently classified as stem-sarcopterygians, may instead be stem-actinopterygians, or even stem-osteichthyans, with implications for the nature of the ancestral bony fish and timing of osteichthyan diversification.