The evolution of dermal shield vascularization in Testudinata and Pseudosuchia: phylogenetic constraints versus ecophysiological adaptations

Abstract

Studies on living turtles have demonstrated that shells are involved in the resistance to hypoxia during apnea via bone acidosis buffering; a process which is complemented with cutaneous respiration, transpharyngeal and cloacal gas exchanges in the soft-shell turtles. Bone acidosis buffering during apnea has also been identified in crocodylian osteoderms, which are also known to employ heat transfer when basking. Although diverse, many of these functions rely on one common trait: the vascularization of the dermal shield. Here, we test whether the above ecophysiological functions played an adaptive role in the evolutionary transitions between land and aquatic environments in both Pseudosuchia and Testudinata. To do so, we measured the bone porosity as a proxy for vascular density in a set of dermal plates before performing phylogenetic comparative analyses. For both lineages, the dermal plate porosity obviously varies depending on the animal lifestyle, but these variations prove to be highly driven by phylogenetic relationships. We argue that the complexity of multi-functional roles of the post-cranial dermal skeleton in both Pseudosuchia and Testudinata probably is the reason for a lack of obvious physiological signal, and we discuss the role of the dermal shield vascularization in the evolution of these groups. This article is part of the theme issue ‘Vertebrate palaeophysiology’.

Vertebrate palaeophysiology

“…They suggest a new hypothesis according to which the functional significance of the origin of the archosaurian four-chambered heart (and the concomitant high systemic blood pressures) may be related to the efficient perfusion of osteoderms to buffer acidosis [3]. Clarac et al [4] posit that osteoderm-mediated calcium buffering in carapaced turtles and archosaurs, as well as thermoregulation, may be limited by vascularization of the dermal skeleton, a feature that is readily interpretable in extinct species based on the fossilized vascular spaces preserved in osteoderms. Surprisingly, they did not find a significant association between osteoderm vascular variation and lifestyle.…”

“…Surprisingly, they did not find a significant association between osteoderm vascular variation and lifestyle. They conclude that the broadly constant high osteoderm vascularity in semi-aquatic taxa may be the outcome of multifactorial roles and historical constraints [4]. A separate paper by Canoville et al [2] reviews documented occurrences of a sex-specific, physiologically unique endosteal tissue known as 'medullary bone', found in reproductive female birds and hypothesized to have existed in some non-avian avemetatarsalians [18,19].…”

“…'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]).…”

Lizards and snakes from the earliest Miocene of Saint-Gérand-le-Puy, France: an anatomical and histological approach of some of the oldest Neogene squamates from Europe

“…We also show, however, that the more dorsally situated fine meshwork of channels of the Ophisaurus holeci parietal table connect with larger antero-posteriorly extending channels, and them opening up into larger cavities or sinuses underneath the smooth area posterior to the parietal table, giving the bone a more porous appearance. This particular vascular arrangement could indicate some thermoregulatory function (see [ 136 ] for potential functions of heavily vascularized ornamented bones in other tetrapods), where the ornamented parietal table could serve as a heat sink/collector and the larger sinuses could serve a storage or rapid drainage function of heated or cooled blood. However, comparative physiological studies using extant anguines such as Ophisaurus spp., Pseudopus apodus , and the fossils are needed to shed light on whether or what function the strong parietal vascularization has in these lizards.…”

Identifying medullary bone in extinct avemetatarsalians: challenges, implications and perspectives

“…Crocodilians, which are the closest relatives to birds among extant amniotes, rely on a different source of calcium for the production of their calcified eggshell. Studies have shown that female alligators do not form MB [21], but rather use the mineral stored in their osteoderms (which are hypothesized to have a physiological, rather than a structural function in crocodilians; see [27][28][29][30][31]) to form the calcified eggshell [32].…”