Dermal bone in early tetrapods: a palaeophysiological hypothesis of adaptation for terrestrial acidosis

Abstract

The dermal bone sculpture of early, basal tetrapods of the Permo-Carboniferous is unlike the bone surface of any living vertebrate, and its function has long been obscure. Drawing from physiological studies of extant tetrapods, where dermal bone or other calcified tissues aid in regulating acid-base balance relating to hypercapnia (excess blood carbon dioxide) and/or lactate acidosis, we propose a similar function for these sculptured dermal bones in early tetrapods. Unlike the condition in modern reptiles, which experience hypercapnia when submerged in water, these animals would have experienced hypercapnia on land, owing to likely inefficient means of eliminating carbon dioxide. The different patterns of dermal bone sculpture in these tetrapods largely correlates with levels of terrestriality: sculpture is reduced or lost in stem amniotes that likely had the more efficient lung ventilation mode of costal aspiration, and in small-sized stem amphibians that would have been able to use the skin for gas exchange.

A quantitative assessment of bone area increase due to ornamentation in the Crocodylia

“…However, the actual role of the superficial, outer blood vessels topographically related to ornamentation, but in limited contact with subjacent bones, remains obscure and conjectural. For this reason, although Janis et al's () hypothesis is not contradictory (but rather in agreement) with the results of the present study, it should be considered with some caution until further documented.…”

“…For instance, pits house a rich vascular supply (Seidel, ; Farlow et al, ; Witzmann et al, ) that would either accelerate blood heating by direct exposition to sun radiations through overlying cutaneous layers, or facilitate heat dissipation by increasing skin perfusion in cool water or shade (see also on this topic Johnson et al, ; Smith et al, ; Robertson and Smith, ; Smith, ; Seebacher and Franklin, ). Although the geometric organization of these vascular bundles remains to be established on detailed, 3D micro‐angiographic studies, it can be hypothesized that, an increase in bone area through ornamentation should necessarily result in a proportional increase in the local amount of superficial blood vessels, and finally improve the efficiency of heat capitation. The occurrence of extensive, superficial vascularization related to bone sculpturing could also be considered in light of Janis et al's () hypothesis attributing to ornamentation, and to the blood vessels associated with it, a role in the control of the acidosis process supposed to have occurred in the blood of basal amniotes incipiently adapting to life on dry land. By extension, this hypothesis could involve also extant diving or aquatic tetrapods.…”

“…However, despite its frequency, the functional significance of this feature is poorly understood. Several hypotheses have been proposed to answer that question: better resistance to mechanical stress (Coldiron, ); augmenting bone‐dermis contact and thus improving skin anchorage (Romer, ; Witzmann et al, ); facilitating cutaneous respiration (Bystrow, ); increasing basking efficiency in ectothermic vertebrates (Seidel, ), or contributing to buffer respiratory acidosis in early land‐dwelling vertebrates and, more generally, semiaquatic tetrapods (Janis et al, ). The last two hypotheses are supported by the occurrence of a rich vascular supply topographically related to bone ornamentation (Witzmann et al, ).…”

Comparative data on the differentiation and growth of bone ornamentation in gnathostomes (Chordata: Vertebrata)

“…Since Bystrow's pioneer works (1935, 1947), at least five hypotheses have been proposed to explain the functional significance of this character. In brief, bone ornamentation could be involved in: a) reinforcement of skin anchorage onto bone (Witzmann, ; Witzmann et al, ), b) improvement of cutaneous respiration (Bystrow, ), c) prevention of blood acidosis (Janis et al, ), d)mechanical strengthening of the bones (Coldiron, , Rinehart and Lucas, ) and, e) improvement of thermoregulation (Seidel, ; Clarac et al, ). Criticizing each of these hypotheses is beyond the scope of this article (see critical synthesis in Clarac et al ).…”

Preferential intracellular pH regulation: hypotheses and perspectives

“…Consequently, we propose that many other vertebrates, including those that exhibit coupled pH regulation as adults, may rely exclusively on preferential pH i regulation during development; an area clearly worthy of further investigation. Finally, we hypothesize that the retention of preferential pH i regulation may have been an exaptation for a number of important evolutionary transitions in vertebrates, including the invasion of freshwater, the evolution of air breathing and the transition to land, events where acid-base homeostasis would otherwise be impaired Janis et al, 2012;Shartau and Brauner, 2014). The specific cellular and molecular mechanisms of preferential pH i regulation are currently unknown and represent a fascinating opportunity for further investigation.…”