Diverse stem-chondrichthyan oral structures and evidence for an independently acquired acanthodid dentition

The teeth of sharks famously form a series of transversely organized files with a conveyor-belt replacement that are borne directly on the jaw cartilages, in contrast to the dermal plate-borne dentition of bony fishes that undergoes site-specific replacement. A major obstacle in understanding how this system evolved is the poorly understood relationships of the earliest chondrichthyans and the profusion of morphologically and terminologically diverse bones, cartilages, splints and whorls that they possess. Here, we use tomographic methods to investigate mandibular structures in several early branching ‘acanthodian’-grade stem-chondrichthyans. We show that the dentigerous jaw bones of disparate genera of ischnacanthids are united by a common construction, being growing bones with non-shedding dentition. Mandibular splints, which support the ventro-lateral edge of the Meckel's cartilage in some taxa, are formed from dermal bone and may be an acanthodid synapomorphy. We demonstrate that the teeth of Acanthodopsis are borne directly on the mandibular cartilage and that this taxon is deeply nested within an edentulous radiation, representing an unexpected independent origin of teeth. Many or even all of the range of unusual oral structures may be apomorphic, but they should nonetheless be considered when building hypotheses of tooth and jaw evolution, both in chondrichthyans and more broadly.

Cellular and molecular mechanisms of frontal bone development in spotted gar (Lepisosteus oculatus)

BackgroundThe molecular mechanisms initiating vertebrate cranial dermal bone formation is a conundrum in evolutionary and developmental biology. Decades of studies have determined the developmental processes of cranial dermal bones in various vertebrate species, finding possible inducers of dermal bone. However, the evolutionarily derived characters of current experimental model organisms hinder investigations of the ancestral and conserved mechanisms of vertebrate cranial dermal bone induction. Thus, investigating such mechanisms with animals diverging at evolutionarily crucial phylogenetic nodes is imperative.ResultsWe investigated the cellular and molecular foundations of skull frontal bone formation in the spotted gar Lepisosteus oculatus, a basally branching actinopterygian. Whole-mount bone and cartilage stainings and hematoxylin-eosin section stainings revealed that mesenchymal cell condensations in the frontal bone of spotted gar develop in close association with the underlying cartilage. We also identified novel aspects of frontal bone formation: Upregulation of F-actin and plasma membrane in condensing cells, and extension of podia from osteoblasts to the frontal bone, which may be responsible for bone mineral transport.ConclusionThis study highlights the process of frontal bone formation with dynamic architectural changes of mesenchymal cells in spotted gar, illuminating supposedly ancestral and likely conserved developmental mechanisms of skull bone formation among vertebrates.

Dental diversity in early chondrichthyans and the multiple origins of shedding teeth

The teeth of sharks famously form a series of parallel, continuously replacing files borne directly on the mandibular cartilages. In contrast, bony fishes possess site-specific shedding dentition borne on dermal plates. Understanding how these disparate systems evolved is challenging, not least because of poorly understood relationships and the profusion of morphologically and terminologically diverse bones, splints and whorls seen in the earliest chondrichthyans. Here we use tomographic methods to investigate the nature of mandibular structures in several early branching ‘acanthodian’-grade stem-chondrichthyans. We characterise the gnathal plates of ischnacanthids as growing bones, and draw similarities between early chondrichthyan and stem gnathostome teeth and jaws. We further build the case for Acanthodopsis, a Carboniferous taxon, as an acanthodid, and show that, unexpectedly, its teeth are borne directly on the mandibular cartilage. Mandibular splints are formed from dermal bone and appear to be an acanthodid synapomorphy. The development of a unidirectionally growing dentition may be a feature of the chondrichthyan total-group. More generally, ischnacanthid and stem gnathostome gnathal plates share a common construction and are likely homologous, and shedding teeth evolved twice in gnathostomes.

Palaeophysiology of pH regulation in tetrapods

The involvement of mineralized tissues in acid–base homeostasis was likely important in the evolution of terrestrial vertebrates. Extant reptiles encounter hypercapnia when submerged in water, but early tetrapods may have experienced hypercapnia on land due to their inefficient mode of lung ventilation (likely buccal pumping, as in extant amphibians). Extant amphibians rely on cutaneous carbon dioxide elimination on land, but early tetrapods were considerably larger forms, with an unfavourable surface area to volume ratio for such activity, and evidence of a thick integument. Consequently, they would have been at risk of acidosis on land, while many of them retained internal gills and would not have had a problem eliminating carbon dioxide in water. In extant tetrapods, dermal bone can function to buffer the blood during acidosis by releasing calcium and magnesium carbonates. This review explores the possible mechanisms of acid–base regulation in tetrapod evolution, focusing on heavily armoured, basal tetrapods of the Permo-Carboniferous, especially the physiological challenges associated with the transition to air-breathing, body size and the adoption of active lifestyles. We also consider the possible functions of dermal armour in later tetrapods, such as Triassic archosaurs, inferring palaeophysiology from both fossil record evidence and phylogenetic patterns, and propose a new hypothesis relating the archosaurian origins of the four-chambered heart and high systemic blood pressures to the perfusion of the osteoderms. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

Origins of bone repair in the armour of fossil fish: response to a deep wound by cells depositing dentine instead of dermal bone

The outer armour of fossil jawless fishes (Heterostraci) is, predominantly, a bone with a superficial ornament of dentine tubercles surrounded by pores leading to flask-shaped crypts (ampullae). However, despite the extensive bone present in these early dermal skeletons, damage was repaired almost exclusively with dentine. Consolidation of bone, by dentine invading and filling the vascular spaces, was previously recognized in Psammolepis and other heterostracans but was associated with ageing and dermal shield wear (reparative). Here, we describe wound repair by deposition of dentine directly onto a bony scaffold of fragmented bone. An extensive wound response occurred from massive deposition of dentine (reactionary), traced from tubercle pulp cavities and surrounding ampullae. These structures may provide the cells to make reparative and reactionary dentine, as in mammalian teeth today in response to stimuli (functional wear or damage). We suggest in Psammolepis , repair involved mobilization of these cells in response to a local stimulatory mechanism, for example, predator damage. By comparison, almost no new bone is detected in repair of the Psammolepis shield. Dentine infilling bone vascular tissue spaces of both abraded dentine and wounded bone suggests that recruitment of this process has been evolutionarily conserved over 380 Myr and precedes osteogenic skeletal repair.