Investigation of a bone lesion in a gorgonopsian (Synapsida) from the Permian of Zambia and periosteal reactions in fossil non-mammalian tetrapods

Abstract

While only distantly related to mammals, the anatomy of Permian gorgonopsians has shed light on the functional biology of non-mammalian synapsids and on the origins of iconic ‘mammal-like’ anatomical traits. However, little is known of gorgonopsian behaviour or physiology, which would aid in reconstructing the paleobiological context in which familiar mammalian features arose. Using multi-modal imaging, we report a discrete osseous lesion in the forelimb of a late Permian-aged gorgonopsian synapsid, recording reactive periosteal bone deposition and providing insights into the origins and diversity of skeletal healing responses in premammalian synapsids. We suggest that the localized lesion on the anterolateral (preaxial) shaft of the left radius represents acute periostitis and, conservatively, most likely developed as a subperiosteal haematoma with subsequent bone deposition and limited internal remodelling. The site records an inner zone of reactive cortical bone forming irregular to radial bony spicules and an outer, denser zone of slowed subperiosteal bone apposition, all of which likely occurred within a single growing season. In surveys of modern reptiles—crocodylians, varanids—such haematomas are rare compared to other documented osteopathologies. The extent and rapidity of the healing response is reminiscent of mammalian and dinosaurian bone pathologies, and may indicate differing behaviour or bone physiology compared to non-dinosaurian reptiles. This report adds to a growing list of putative disease entities recognized in early synapsids and broadens comparative baselines for pathologies and the evolution of bone response to disease in mammalian forebears. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

Vertebrate palaeophysiology

“…For example, acute skeletal diseases in birds may be frequently accompanied by granular or caseous abscesses because, unlike humans and other mammals, they do not accumulate pus [38]. In this context, the contributions of Jentgen-Ceschino et al [12] and Kato et al [13] explore the aetiologies of reactive periosteal bone in three separate cases in the archosaur and synapsid lineages, respectively. The exciting results of both studies suggest avian-and mammal-like disease responses-rather than 'reptile-like'-in some extinct dinosaurs and synapsids.…”

“…'Vertebrate palaeophysiology' will promote a better understanding of how organism-environment interactions have evolved in terms of energy budgets, predator-prey relationships and sensitivity to environmental change. The research areas covered by this theme issue include: phospho-calcic metabolism [2], acid-base homeostasis [3,4], thermometabolism [4][5][6][7][8][9], respiratory physiology [10], skeletal growth [11], palaeopathophysiology [12,13], genome size and metabolic rate [14], and a concluding historical perspective [15]. Sometimes, the two components ( physiological mechanism and palaeobiological inference) are proposed in separate papers (for instance, three contributions devoted to mechanisms of thermogenesis mechanisms [5][6][7] and three papers dealing with the thermometabolic inferences in extinct taxa [4,8,9]).…”

Case study of radial fibrolamellar bone tissues in the outer cortex of basal sauropods

“…Recently, some palaeopathology studies have investigated the bone internal structure systematically with modern imaging techniques (e.g. [48,109,110]) as it can be the only relevant source of data in some palaeopathologies (e.g. intervertebral fusion [89,111,112]).…”

“…Radiography is considered less valuable than CT scans regarding the diagnostic details that can be obtained [65] and, even though pathological bones may be identified at the macroscopic scale, internal anatomy provides most evidence to discriminate successfully the pathology (e.g. [106,110]). Bone histology is somehow discarded in favour of imaging techniques like CT scans because royalsocietypublishing.org/journal/rstb Phil.…”

The First Healed Bite Mark and Embedded Tooth in the Snout of a Middle Permian Gorgonopsian (Synapsida: Therapsida)

“…The paleopathological study of extinct species is the gateway to many, otherwise inaccessible, paleobiological traits such as intraspecific behavior (Farke et al, 2009;Peterson and Vittore, 2012;Peterson et al, 2013), diet and food acquisition (DePalma et al, 2013), etiology and healing capabilities (Wolff et al, 2009;Kato et al, 2020), soft tissue reconstruction (Rega et al, 2012), thermophysiology (Benoit et al, 2015), interspecific interactions (Aureliano et al, 2021), biting force (Erickson et al, 1996;Gignac et al, 2010), and even key transitional events in the evolutionary history of vertebrates such as the onset of arboreality in hominins and terrestriality in early tetrapods (Bishop et al, 2015;Kappelman et al, 2016).…”