Vertebrate palaeophysiology

Abstract

Physiology is a functional branch of the biological sciences, searching for general rules by which explanatory hypotheses are tested using experimental procedures, whereas palaeontology is a historical science dealing with the study of unique events where conclusions are drawn from congruence among independent lines of evidence. Vertebrate palaeophysiology bridges these disciplines by using experimental data obtained from extant organisms to infer physiological traits of extinct ones and to reconstruct how they evolved. The goal of this theme issue is to understand functional innovations imprinted on modern vertebrate clades, and how to infer (or ‘retrodict’) physiological capacities in their ancient relatives a posteriori. As such, the present collection of papers deals with different aspects of a rapidly growing field to understand innovations in: phospho-calcic metabolism, acid–base homeostasis, thermometabolism, respiratory physiology, skeletal growth, palaeopathophysiology, genome size and metabolic rate, and it concludes with a historical perspective. Sometimes, the two components (physiological mechanism and palaeobiological inference) are proposed in separate papers. Other times, the two components are integrated in a single paper. In all cases, the approach was comparative, framed in a phylogenetic context, and included rigorous statistical methods that account for evolutionary patterns and processes.

This article is part of the theme issue ‘Vertebrate palaeophysiology’.

1. Introduction

Mayr [1] stated that biological research can be divided into two main areas that differ in method and basic concepts: functional biology aims to answer ‘how does it work?’ and uses experimental approaches to decipher proximal causes, whereas evolutionary biology is concerned with ‘how did it appear?’ and mainly uses the comparative method to identify ultimate causes. Typically, physiology belongs to the area of functional biology: it searches for general rules by which explanatory hypotheses are tested using experimental procedures. The refutability of hypotheses and repeatability of experiments are cornerstones of this approach. By contrast, modern palaeontology is a subdiscipline of evolutionary biology. It is a historical science dealing with the study of unique events. Conclusions are based on congruence among independent lines of evidence. The field of vertebrate palaeophysiology bridges these disciplines by using experimental data obtained in extant organisms to infer physiological traits of extinct ones. These inferences are usually performed in a phylogenetic context to avoid the non-independence among observations and are predicted upon uniformitarianism, according to which the same natural laws that operate in the present have operated in the past. This special issue synthesizes recent conceptual and methodological advances that have substantially improved our understanding of the physiology of extinct taxa. This issue forms a much needed cross-pollination of the basic science fields of physiology and vertebrate palaeontology. It creates a synergy among its articles dealing with physiological mechanisms while revealing new developments in palaeobiological inference. Palaeobiologists, palaeontologists and evolutionary biologists will be interested in the discoveries of vertebrate palaeophysiology presented in this special issue because the processes (e.g. thermoregulation, acid–base regulation, calcium homeostasis) are tightly related to the morphology, lifestyle, behaviour and ecology of extinct vertebrates. ‘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 [4–9], 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 [5–7] and three papers dealing with the thermometabolic inferences in extinct taxa [4,8,9]). Other times, the two components are integrated in a single paper (e.g. palaeophysiology of pH regulation in early tetrapods; [3]). We deliberately omitted the field of biomechanics (dealing with the effect of biomechanical constraints on the structure of bone tissue and the use of these structures to infer the locomotion types of extinct vertebrates) because an abundant literature exists on this topic.

2. Mineralized tissue homeostasis and acid–base regulation

Acid–base regulation and mineral homeostasis are important and related functions that involve balance of blood, extracellular and intracellular fluid pH, and modulation of ions and bicarbonate to buffer acid–base disturbances [16]. These processes are of particular interest in the first terrestrial tetrapods and in secondarily aquatic tetrapods owing to frequent periods of metabolic and respiratory acidoses, especially during exercise (because the respiratory systems are not optimal for terrestrial lifestyle in the former and because of apnoea during diving in the latter) [16,17]. Acidosis can be buffered by using stored calcium and magnesium carbonates from dermal bone [16,17]. Janis et al. [3] provide readers with additional evidence for these mechanisms and argue that perfusing dermal bones may have played an important role to buffer acidosis. 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. 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]. This tissue is widely regarded as a short-term calcium store available for shelling eggs [20,21]. The authors summarize progress in diagnosing medullary bone, while highlighting recent and emerging work on biochemical signatures, among other important criteria, that support its recognition in fossils.

3. Thermometabolism

A section on the study of thermometabolism and thermoregulation reviews its physiological mechanisms in vertebrates and palaeobiological inference within the extant phylogenetic bracket of modern endotherms (i.e. birds and most mammal species). The acquisition of endothermy is one of the most significant innovations in vertebrate physiology. It modified the energetic relationships between organisms and their environments [22], lifted constraints on external thermal thresholds both temporally and spatially (e.g. activity patterns, latitudinal gradients) [23], and probably coincided with a suite of changes in major organ systems involved in respiration and circulation that prevail in the majority of terrestrially active (and many secondarily aquatic) vertebrate species [24,25]. At the ecosystem level, it imposed a restructuring of animal communities along trophic webs [26]. The fossil record documents major shifts in these biological systems spanning the Permian through to Triassic periods, and parsimony suggests that mammalian and avian endothermy evolved convergently—birds and mammals are two distantly related tetrapod groups whose last common ancestor (ca 320 Ma) was most probably ectothermic.

Two thermogenetic mechanisms are analysed in the theme issue. On the one hand, mitochondria of brown adipose tissue produce heat by uncoupling food-derived substrate oxidation from chemical energy (ATP) production in many eutherian mammals [27,28]. It has been shown that various physiological factors, including exercise, diet and the immune system, can cause the browning of white adipose tissue through epigenetic mechanisms [29]. In the first contribution of this section, Jastroch & Seebacher [5] review the molecular mechanisms underlying the browning of white adipocytes, and their potential contribution to endogenous heat production in the evolution of endothermy. Bal & Periasamy [6] review another mechanism of non-shivering thermogenesis: inhibition of Ca²⁺ transport, but not ATP hydrolysis, of sarco-endoplasmic reticulum calcium ATPase (SERCA) by sarcolipin, resulting in a futile pump activity that generates heat. The contribution by Legendre & Davesne [7] surveys the homoplasic distribution of mechanisms involved in non-shivering thermogenesis across vertebrate phylogeny. The authors argue that ‘endothermy’ in birds and mammals is often inconsistently defined, and may represent evolutionarily labile mechanisms that permit endogenous thermogenesis convergently in different clades.

Cubo & Faure-Brac [9] perform retrodictions of the thermometabolism of extinct synapsids using phylogenetic eigenvector maps, a recently developed comparative method. Based on a phylogenetic bracket of extant tetrapods, they establish a baseline relationship between vascular histometrics in cortical bone and resting metabolic rate, and suggest that some late Permian therapsids might have had resting metabolic rates comparable to extant endothermic mammals exhibiting similar histology in contrast with more basal synapsids (Varanopidae, Edaphosauridae, Ophiacodontidae Sphenacodontidae). Prior studies have argued that other vascular parameters, particularly canal sizes and densities that impact O₂ diffusive capacity, reflected an expansion of aerobic scope in some Triassic therapsids and contemporary archosauromorphs that may or may not have been coincident with changes in thermoregulatory abilities [30]. The present authors conclude that palaeohistology reveals independent acquisition of endotherm-like resting metabolic rates in at least three amniote lineages: Therapsida, Sauropterygia and Archosauromorpha [9]. Stable isotope biogeochemistry helps to catalogue the fossil record of thermometabolism as a test of these hypotheses. A previous analysis of the thermophysiology of marine reptiles showed that Plesiosauria, Ichthyosauria and (probably) Mosasauridae were endotherms [31]. Results obtained by Séon et al. [8] for Thalattoshuchia (marine crocodylomorphs) are consistent with hydroxyapatite formed under temperatures intermediate between those of ectotherms and endotherms, and behavioural adjustments are speculated to have played a role in their thermoregulation.

4. Respiration and cardiopulmonary systems

Vertebrate respiratory and cardiopulmonary systems are specialized both for bulk convection and diffusion of gases that make possible the elimination of CO₂ and uptake of O₂ for cellular respiration. Modifications to these systems in the synapsid and archosaur lineages, which include wide-ranging foragers and terrestrial cursors, probably promoted the expansion of aerobic scope and athleticism previously unseen in vertebrates prior to the Permo-Triassic boundary. Brocklehurst et al. [10] analyse the evolution of ventilation mechanics, as well as the osteological correlates for lung structure and distribution of air sacs, in archosaurs.

5. Reproduction, growth and life cycle

Growth and reproduction are intricately linked to a variety of physiologic processes. For instance, mammalian- and avian-style parental care and reproduction have been tied to the very origins of endothermy [32,33]. This is because selection for endothermy—whether obligate or seasonally facultative [34]—permits the parent to maintain incubation temperature, thereby promoting brood survival and fitness. Furthermore, endothermic mammals and, especially, birds are known to be capable of relatively faster postnatal growth than similar-sized ectotherms [35], possibly owing to a combination of greater parental investment during early growth, as well as resource use and metabolic processing. The contributions of Canoville et al. [2] and Huttenlocker & Shelton [11] provide insights into early growth and life cycle innovations of avian-line archosaurs and synapsids, respectively. In addition to discussing the typology and histochemistry of medullary bone, Canoville et al. promote its use towards understanding more generally the fascinating reproductive biology of dinosaurs [2]. Better characterization of medullary tissues in reproductive dinosaurs would help palaeontologists identify sexual dimorphism in the fossil record, more accurately estimate growth rate and age at maturity, and understand nesting and rearing behaviour. The transition from aquatic tetrapods to more terrestrialized amniotes, such as basal synapsids, also brought challenges that influenced innovations in growth and life cycle during the late Palaeozoic establishment of land-based vertebrate communities. Huttenlocker & Shelton [11] present a simple cross-sectional study showing prolonged, cyclic growth in basal synapsid limb bones, and reduced bone robusticity reflective of a terrestrial life cycle freed from aquatic resources in a predictable and seasonal climate regime.

6. Palaeopathology

While the following section could form the subject of a separate volume in its own right, the conclusions of palaeopathology—the study of ancient disease—give inference to important physiological and behavioural attributes of extinct animals that cannot otherwise be observed directly. Whereas a vast literature exists on human skeletal disease, zoological palaeopathology posits that knowledge of human disease is entirely inadequate to diagnose animal disease and to explain the mechanisms of healing in vertebrate clades separated by millions of years of evolution [36,37]. 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. Nonetheless, these cases highlight important caveats of cross-clade comparisons and reinforce the need for ongoing sampling of fossil and extant baselines, multi-modal data acquisition and coordinated efforts by palaeopathologists to index these datasets that could improve diagnostic rigour in fossils.

7. Synthesis: inferring physiological capacities in extinct vertebrates

While elucidating the origins of physiological traits remains an important component of evolutionary physiology, limitations endure that constrain our ability to reconstruct the physiological capacities of extinct organisms with confidence. This is largely because form can be directly observed from fossilized tissues, whereas function is inferred within a framework of comparative anatomy, biophysics and phylogenetic bracketing. Each requires reasonably large comparative datasets (including extant training datasets), precision measurements and an accepted evolutionary model that is ratcheted to the fossil data (whether morphological, histological or biogeochemical). The final contributions of Gardner et al. [14] and Padian & de Ricqlès [15] address these theoretical limitations within quantitative and more philosophical contexts. Gardner et al. [14] test the hypothesis of a causal relationship between genome size and basal metabolic rate. This hypothesis is based on the postulate suggesting that nucleus size (and cell size) may have an effect on cellular metabolism through, for example, surface area-to-volume ratios or differences in GC content. The contributors did not find support for a direct functional relationship between genome size and basal metabolic rate in extant vertebrates using Bayesian phylogenetic statistical analysis [14]. The essay of Padian & de Ricqlès [15] offers a critique of practical approaches to palaeophysiology. These approaches, the authors argue, are limited to correlative factors inferred from fossilizable tissues under a modern framework that encompasses only two binary categories—‘cold-blooded’ fishes, amphibians and reptiles, and ‘warm-blooded’ birds and mammals—which inadequately describe the breadth of physiological strategies available to vertebrates. In addition to the large-scale phylogenetic comparative studies such as those of Cubo et al. [39] and Gardner et al. [14], which attempt to control for the effects of phylogeny, focused clade-specific studies that further control for body size, age to maturity and growth rate, environmental context and interelemental histovariability (e.g. histovariation in Haversian replacement; [40]) shed further light on physiologic capacities in extinct groups.

Biographies

Editor biographies

Jorge Cubo is a professor of Palaeontology at Sorbonne University, Paris, France. He received his PhD in bone biomechanics from the University of Barcelone, Spain, in 1997. His work centres on palaeobiological inferences of thermometabolism in amniotes using bone histology in a phylogenetic context. He has pioneered the use of phylogenetic comparative methods in comparative bone histology. Photography: © MNHN-Agnès Iatzoura.

Adam Huttenlocker is an assistant professor of Integrative Anatomical Sciences at the University of Southern California, Los Angeles, USA. He received his PhD in palaeobiology from the University of Washington, Seattle, in 2013, and from 2013 to 2016 held a prestigious National Science Foundation Postdoctoral Fellowship at the University of Utah, Salt Lake City, to investigate palaeophysiology and energetics in fossil tetrapods. His research combines functional anatomy, medical imaging and hard-tissue histology in order to understand skeletal function, growth and the origins of endothermic physiology in mammals and their extinct synapsid forebears.

Data accessibility

This article has no additional data.

Authors' contributions

J.C. and A.K.H. wrote the paper.

Competing interests

The authors declare no competing interests.

Funding

We received no funding for this study.