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

Abstract

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.

Osteohistology of Greererpeton provides insight into the life history of an early Carboniferous tetrapod

“…Histological studies from the intervening Carboniferous Period are largely lacking, due to the rarity of tetrapod fossils preserved in Mississippian rock (Anderson et al, 2015; Clack, 2002; Coates & Clack, 1995; Otoo et al, 2019; Romer, 1956; Warren & Turner, 2004). Other than two studies examining pathological bone (Bishop et al, 2015; Herbst et al, 2019) and vertebral elements in a few Carboniferous taxa (Danto et al, 2016, 2017), there is a scarcity of osteohistological data for nearly 60 million years of tetrapod evolution (Figure 1). However, it is during this time period that the critical transition from fully aquatic to fully terrestrial tetrapods is inferred to have taken place (Dickson et al, 2021; Figure 1).…”

Intracortical remodelling increases in highly-loaded bone after exercise cessation

“…Bone repair without resorption .U values tend towards 0 as the overlap between the two groups' rank distributions decreases to 0. All groups have n = 6 except rested tibia and rested metacarpal diaphysis which have n may occur by organic and inorganic substrates bridging and sealing cracks [30,47], which might be an inherent property of mineralised tissues occurring across all vertebrate taxa like bone remodelling is [48]. In vitro mechanical testing of bone specimens machined from the third metacarpal of Thoroughbred racehorses showed that the elastic modulus and yield strength of specimens were not significantly affected by prior fatigue loading equivalent to a lifetime of racing [49].…”

Mechanisms of dermal bone repair after predatory attack in the giant stem‐group teleost Leedsichthys problematicus Woodward, 1889a (Pachycormiformes)

“…This represents growing circumvascular bone. Thus, a developmental series can be proposed following damage: (1) an initial (hypothetical) inflammatory phase and formation of a haematoma (Maruyama et al, 2020, although not as large a response as in mammal repair [Moss, 1962; Herbst et al, 2019]); (2) blood vessels enter the area, with osteoclasts resorbing original bone to prepare a margin for new bone deposition (vascular response being crucial in mammalian bone healing; Tomlinson & Silva, 2013); (3) osteoblasts at this resting surface deposit woven bone that entraps the anchoring fibres, normal to these intrinsic fibres, and thicker; (4) woven bone surrounds vascular canals; (5) the size of the vascular canal decreases with layers of organised bone surrounding the canal space, representing the circumvascular bone; (6) all woven bone is eventually resorbed and only organised, fine fibered bone remains.…”