Locomotory behaviour of early tetrapods from Blue Beach, Nova Scotia, revealed by novel microanatomical analysis

Evidence for terrestriality in early tetrapods is fundamentally contradictory. Fossil trackways attributed to early terrestrial tetrapods long predate the first body fossils from the Late Devonian. However, the Devonian body fossils demonstrate an obligatorily aquatic lifestyle. Complicating our understanding of the transition from water to land is a pronounced gap in the fossil record between the aquatic Devonian taxa and presumably terrestrial tetrapods from the later Early Carboniferous. Recent work suggests that an obligatorily aquatic habit persists much higher in the tetrapod tree than previously recognized. Here, we present independent microanatomical data of locomotor capability from the earliest Carboniferous of Blue Beach, Nova Scotia. The site preserves limb bones from taxa representative of Late Devonian to mid-Carboniferous faunas as well as a rich trackway record. Given that bone remodels in response to functional stresses including gravity and ground reaction forces, we analysed both the midshaft compactness profiles and trabecular anisotropy, the latter using a new whole bone approach. Our findings suggest that early tetrapods retained an aquatic lifestyle despite varied limb morphologies, prior to their emergence onto land. These results suggest that trackways attributed to early tetrapods be closely scrutinized for additional information regarding their creation conditions, and demand an expansion of sampling to better identify the first terrestrial tetrapods.

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’.

The Invasion of Land

Basal stem tetrapods were fully aquatic but spent time at the water surface breathing air, which was useful at the end of the Devonian, when aquatic oxygen levels were low. After the Devonian, early tetrapods became fully terrestrial, at least as adults. This transition involved major changes in the musculoskeletal system for locomotion and the evolution of new modes of feeding. Aerial vision required changes in the eye but then allowed for high-resolution vision over long distances. In contrast, the lateral line systems are useless in air and were lost in fully terrestrial tetrapods. The brains of early tetrapods were relatively simple, possibly simplified through a process called paedomorphosis. The telencephalon’s main function in early tetrapods was to inhibit or disinhibit the lower brain regions. Later tetrapods diverged into extant amphibians and amniotes. Within the amphibian lineage, anurans evolved a tympanic ear, which increased their ability to hear airborne sounds.

Bony lesions in early tetrapods and the evolution of mineralized tissue repair

Bone healing is an important survival mechanism, allowing vertebrates to recover from injury and disease. Here we describe newly recognized paleopathologies in the hindlimbs of the early tetrapods Crassigyrinus scoticus and Eoherpeton watsoni from the early Carboniferous of Cowdenbeath, Scotland. These pathologies are among the oldest known instances of bone healing in tetrapod limb bones in the fossil record (about 325 Ma). X-ray microtomographic imaging of the internal bone structure of these lesions shows that they are characterized by a mass of trabecular bone separated from the shaft's trabeculae by a layer of cortical bone. We frame these paleopathologies in an evolutionary context, including additional data on bone healing and its pathways across extinct and extant sarcopterygians. These data allowed us to synthesize information on cell-mediated repair of bone and other mineralized tissues in all vertebrates, to reconstruct the evolutionary history of skeletal tissue repair mechanisms. We conclude that bone healing is ancestral for sarcopterygians. Furthermore, other mineralized tissues (aspidin and dentine) were also capable of healing and remodeling early in vertebrate evolution, suggesting that these repair mechanisms are synapomorphies of vertebrate mineralized tissues. The evidence for remodeling and healing in all of these tissues appears concurrently, so in addition to healing, these early vertebrates had the capacity to restore structure and strength by remodeling their skeletons. Healing appears to be an inherent property of these mineralized tissues, and its linkage to their remodeling capacity has previously been underappreciated.

Palate and braincase ofWhatcheeria deltaeLombard & Bolt, 1995

ABSTRACTThe reconstructed palate ofWhatcheeria deltaeindicates a skull that was unusually narrow: at least 2.2 times longer than wide if the pterygoids are conservatively placed in the horizontal plane. This maximum width is narrower than any other early tetrapod reconstructed so far. Rotating the pterygoids to produce a vaulted palate would produce an even narrower skull. Primitive palatal features include very narrow interpterygoid vacuities and a vomer, palatine, and ectopterygoid with fang-sized replacement pairs. It is derived in that there is no anterior palatal fenestra and the premaxilla has a substantial palatal shelf – a combination of characters shared only with Proterogyrinus among early tetrapods. There is a possible septomaxilla in one specimen.Whatcheeriadiffers from and is more derived thanPederpes, its likely sister taxon, in that only the pterygoid is covered with denticles, the vomer, palatine, and ectopterygoid containing labyrinthine teeth only. Reconstructed dental occlusion indicates that the large choana apparently accommodated the large dentary fangs; this would be a unique feature among early tetrapods. The palatal ramus of the pterygoid is longer than the quadrate ramus, which does not have a descending flange. Like Meckel's cartilage in the lower jaw, the palatoquadrate is fully ossified in larger specimens, such that in a posterior view of the skull the pterygoid is mostly hidden from sight by the epipterygoid. The ossified neurocranium consists of the basiparasphenoid and basioccipital; no ossified sphenethmoid has been found. Remains of otic capsules are partial, crushed, and smeared, so no useful morphology is available. The stapes appears to be more columnar and less plate-like than in many other primitive, early tetrapods.