Trunk exoskeleton in teleosts is mesodermal in origin

Abstract

The vertebrate mineralized skeleton is known to have first emerged as an exoskeleton that extensively covered the fossil jawless fish. The evolutionary origin of this exoskeleton has long been attributed to the emergence of the neural crest, but experimental evaluation for this is still poor. Here we determine the embryonic origin of scales and fin rays of medaka (teleost trunk exoskeletons) by applying long-term cell labelling methods, and demonstrate that both tissues are mesodermal in origin. Neural crest cells, however, fail to contribute to these tissues. This result suggests that the trunk neural crest has no skeletogenic capability in fish, instead highlighting the dominant role of the mesoderm in the evolution of the trunk skeleton. This further implies that the role of the neural crest in skeletogenesis has been predominant in the cephalic region from the early stage of vertebrate evolution.

Tracing the evolutionary origin of vertebrate skeletal tissues: insights from cephalochordate amphioxus

“…New insights gained from the comparative studies in amphioxus imply the primordial role of somites over neural crest cells in the evolutionary origin of vertebrate skeletal tissues. This idea is consistent with recent findings that the trunk dermal skeletal elements (such as teleost scales and fin rays) are derived from the mesoderm instead of neural crest cells [65 ]). The chondrogenic developmental program in the vertebrate neural crest did not evolve de novo, but is, instead, co-opted in a mosaic manner from a pre-existing chondrogenic repertoire present in the somite and its derivatives.…”

Denticle-embedded ampullary organs in a Cretaceous shark provide unique insight into the evolution of elasmobranch electroreceptors

“…Although elasmoid scales of teleost fishes arise from mesoderm (Lee et al 2013;Mongera and Nüsslein-Volhard 2013;Shimada et al 2013), it cannot be excluded that both mesoderm-derived and neural crest-derived mesenchymal cells contribute to the formation of more ancestral types of scales such as tooth-like placoid scales of cartilaginous fishes (Green et al 2015). As mentioned above, electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes (Gillis et al 2012;Baker et al 2013), not neural-crest derived as previously reported (Freitas et al 2006).…”

Postembryonic staging of wild‐type goldfish, with brief reference to skeletal systems

“…31, 32), it was hypothesized that these fins share a common positional value and patterning mechanism (the so‐called Dorsal + Anal fin patterning module, proposed by Mabee et al, 2002). It is known that the median fin rays and their primordial cells are derived from the somite in medaka (Shimada et al, 2013), suggesting that the anal and dorsal fins of zebrafish and goldfish are also derived from somite derivatives. In summary, it is expected that the anal and dorsal fin rays may be derived from somite‐derived cells in both zebrafish and goldfish, but the timing of mesenchymal cell differentiation has altered between these two lineages.…”