Skeletal histology of Bothriolepis canadensis (Placodermi, Antiarchi) and evolution of the skeleton at the origin of jawed vertebrates

Abstract

We used light microscopy and scanning electron microscopy to compile a complete histological description of the dermal skeleton of the antiarch placoderm, Bothriolepis canadensis. Placodermi is most often cited as the sister group of crown group Gnathostomata, but some recent authors propose that placoderms instead represent a paraphyly of forms leading to the crown. In either phylogenetic scenario, comparative analysis of placoderm and gnathostome histological data allows us to address the primitive condition of both the gnathostome skeleton and the jawed vertebrate skeleton. The results of this work support the interpretation that the external skeleton of Bothriolepis canadensis is comprised exclusively of cellular dermal bone tissue. The unique stratification of the antiarch thoracic skeleton that has led to controversial interpretations in the past is explained by the nature of the articulations between adjacent elements. Skeletal features long thought to be gnathostome innovations are instead discovered to arise along the gnathostome stem. These innovations include secondary osteons, the systematic reconstruction of the skeleton in response to growth, and unfused, overlapping joints that enable marginal growth while maximizing the area of the articulation surface. The extensive evidence for spheritic mineralization agrees with a model of the skeleton as one capable of a high growth rate and active remodeling. Dermal skeletal development in both placoderms and osteichthyans is primarily skeletogenetic with only a minor odontogenetic contribution in some taxa. This demonstrates the problem inherent with assuming a broad application for those hypotheses of dermal skeletal evolution that are based on a chondrichthyan model. Our results highlight the importance of anatomical and ontogenetic context in the interpretation of fossil tissues.

New Insights in the Ontogeny and Taphonomy of the Devonian Acanthodian Triazeugacanthus affinis From the Miguasha Fossil-Lagerstätte, Eastern Canada

“…Despite the excellent state of preservation of bones at the microstructural [49][50][51], histological (Figure 1h,i) and anatomical levels, our results indicate a pervasive recrystallization of bioapatite in Triazeugacanthus skeletal structures. Modification of the mineral composition of fossil bones (e.g., presence of authigenic calcite) from the Escuminac Formation has been previously reported in the placoderm Bothriolepis canadensis and the osteolepiform Eusthenopteron foordi [36].…”

“…However, such type of replacement modifies the structure of the biological material at a micrometric scale (e.g., presence of carbonate-fluorapatite infillings discordant with the biogenic Retzius striae in mammalian tooth enamel [28]). In the Miguasha Fossil-Lagerstätte, the preservation of the bone microstructures [49][50][51]64] could suggest a more subtle transformation mechanism, consistent with an early diagenetic stage, even though the formation of the "francolite"-type environment of substituted carbonates implies a transformation of apatite down to the atomic scale. Therefore, the respective contributions of early transformation and potential slow modifications [65] in the sedimentological environment of the Escuminac Formation have still to be determined.…”

A mathematical model for mechanotransduction at the early steps of suture formation

“…By analysing the microscopic anatomy of sutures in a mammal, a basal actinopterygian and a placoderm, we provide evidence indicating that the mechanisms driving bone deposition in sutures share similarities between extinct ancestral vertebrates and extant mammals [36], and that a set of simple mechanotransduction phenomena may be conserved in all species presenting with dermal bones. In fact, placoderms are considered as the most basal jawed vertebrates and the state of a character within this group can be considered as plesiomorphic for all gnathostomes, including tetrapods [32].…”

A quantitative assessment of bone area increase due to ornamentation in the Crocodylia

“…Bone ornamentation, also referred to as bone sculpture, frequently occurs on dermal bones in many vertebrate taxa, especially those having an aquatic or amphibious lifestyle (Downs and Donoghue, ; Witzmann et al, ;). The most common (though nonunique) form of bone ornamentation consists of pits and interconnected ridges that are distinguishable from « simple » vascular imprints because they occur only on the outer surface of the bones, and tend to constitute a highly repetitive, nonrandom geometrical pattern.…”