Vertebrate Palaeophysiology

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Vertebrate Palaeophysiology

Jorge Cubo, Adam Huttenlocker

To cite this version:

Jorge Cubo, Adam Huttenlocker. Vertebrate Palaeophysiology. Philosophical Transactions of the Royal Society B: Biological Sciences, Royal Society, The, 2020, 375 (1793), pp.20190130.

�10.1098/rstb.2019.0130�. �hal-03143776�

Vertebrate Palaeophysiology Jorge Cubo

and Adam K. Huttenlocker

1

Sorbonne Université, MNHN, CNRS, Centre de Recherche en Paléontologie – Paris (CR2P, UMR 7207), 4 place Jussieu, 75005 Paris, France

2

Department of Integrative Anatomical Sciences, University of Southern California, Los Angeles, California, USA

Keywords: phospho-calcic metabolism, acid-base homeostasis,

thermometabolism, respiratory physiology, growth, palaeopathophysiology

Abstract 0

Physiology is a functional branch of the biological sciences, searching for general rules by 1

which explanatory hypotheses are tested using experimental procedures, whereas 2

palaeontology is a historical science dealing with the study of unique events where conclusions 3

are drawn from congruence among independent lines of evidence. Vertebrate Palaeophysiology 4

bridges these disciplines by using experimental data obtained from extant organisms to infer 5

physiological traits of extinct ones and to reconstruct how they evolved. The goal of this theme 6

issue is to understand functional innovations imprinted on modern vertebrate clades, and how 7

to infer (or ‘retrodict’) physiological capacities in their ancient relatives a posteriori. As such, 8

the present collection of papers deals with different aspects of a rapidly growing field to 9

understand innovations in: phospho-calcic metabolism, acid-base homeostasis, 10

thermometabolism, respiratory physiology, skeletal growth, palaeopathophysiology, genome 11

size and metabolic rate, and it concludes with a historical perspective. Sometimes the two 12

components (physiological mechanism and palaeobiological inference) are proposed in 13

separate papers. Other times, the two components are integrated in a single paper. In all cases 14

the approach was comparative, framed in a phylogenetic context, and included rigorous 15

statistical methods that account for evolutionary patterns and processes.

16

1. Introduction 17

18

Ernst Mayr [1] stated that biological research can be divided into two main areas that differ in 19

method and basic concepts: functional biology aims to answer ‘‘how does it work?’’ and uses 20

experimental approaches to decipher proximal causes, whereas evolutionary biology is 21

concerned with “how did it appear?” and mainly uses the comparative method to identify 22

ultimate causes. Typically, physiology belongs to the area of functional biology: it searches for 23

general rules by which explanatory hypotheses are tested using experimental procedures.

24

Refutability of hypotheses and repeatability of experiments are cornerstones of this approach.

25

In contrast, modern palaeontology is a subdiscipline of evolutionary biology. It is a historical 26

science dealing with the study of unique events. Conclusions are based on congruence among 27

independent lines of evidence. The field of Vertebrate Palaeophysiology bridges these 28

disciplines by using experimental data obtained in extant organisms to infer physiological traits 29

of extinct ones. These inferences are usually performed in a phylogenetic context to avoid the 30

non-independence among observations and are predicated upon uniformitarianism, according 31

to which the same natural laws that operate in the present have operated in the past. This 32

special issue synthesises recent conceptual and methodological advances that have 33

substantially improved our understanding of the physiology of extinct taxa. This issue forms a 34

much needed cross-pollination of the basic science fields of physiology and vertebrate 35

palaeontology. It creates a synergy among its articles dealing with physiological mechanisms 36

while revealing new developments in palaeobiological inference. Palaeobiologists, 37

palaeontologists, and evolutionary biologists will be interested in the discoveries of vertebrate 38

palaeophysiology presented in this special issue because the processes (e.g., thermoregulation, 39

acid-base regulation, calcium homeostasis) are tightly related to the morphology, lifestyle, 40

behaviour, and ecology of extinct vertebrates. “Vertebrate Palaeophysiology” will promote a 41

better understanding of how organism-environment interactions have evolved in terms of 42

energy budgets, predator-prey relationships, and sensitivity to environmental change. The 43

research areas covered by this theme issue include: phospho-calcic metabolism [2], acid-base 44

homeostasis [3, 4], thermometabolism [4-9], respiratory physiology [10], skeletal growth [11], 45

palaeopathophysiology [12, 13], genome size and metabolic rate [14] and a concluding 46

historical perspective [15]. Sometimes the two components (physiological mechanism and 47

palaeobiological inference) are proposed in separate papers (for instance three contributions 48

devoted to mechanisms of thermogenesis mechanisms - [5-7] - and three papers dealing with 49

the thermometabolic inferences in extinct taxa - [4, 8, 9]). Other times, the two components are 50

integrated in a single paper (e.g., palaeophysiology of pH regulation in early tetrapods [3]). We

51

4 deliberately omitted the field of biomechanics (dealing with the effect of biomechanical 52

constraints on the structure of bone tissue and the use of these structures to infer the 53

locomotion types of extinct vertebrates) because an abundant literature exists on this topic.

54 55

2. Mineralized Tissue Homeostasis and Acid-Base Regulation 56

57

Acid-base regulation and mineral homeostasis are important and related functions that involve 58

balance of blood, extracellular and intracellular fluid pH, and modulation of ions and 59

bicarbonate to buffer acid-base disturbances [16]. These processes are of particular interest in 60

the first terrestrial tetrapods and in secondarily aquatic tetrapods due to frequent periods of 61

metabolic and respiratory acidoses, especially during exercise (because the respiratory 62

systems are not optimal for terrestrial lifestyle in the former and because of apnoea during 63

diving in the later) [16, 17]. Acidosis can be buffered by utilizing stored calcium and 64

magnesium carbonates from dermal bone [16, 17]. Janis et al [3] provide readers with 65

additional evidence for these mechanisms and argue that perfusing dermal bones may have 66

played an important role to buffer acidosis. They suggest a new hypothesis according to which 67

the functional significance of the origin of the archosaurian four-chambered heart (and the 68

concomitant high systemic blood pressures) may be related to the efficient perfusion of 69

osteoderms to buffer acidosis [3]. Clarac et al [4] posit that osteoderm-mediated calcium 70

buffering in carapaced turtles and archosaurs, as well as thermoregulation, may be limited by 71

vascularization of the dermal skeleton, a feature that is readily interpretable in extinct species 72

based on the fossilized vascular spaces preserved in osteoderms. Surprisingly, they did not find 73

a significant association between osteoderm vascular variation and lifestyle. They conclude 74

that the broadly constant high osteoderm vascularity in semi-aquatic taxa may be the outcome 75

of multifactorial roles and historical constraints [4].

76

A separate paper by Canoville et al. [2] reviews documented occurrences of a sex- 77

specific, physiologically unique endosteal tissue known as ‘medullary bone,’ found in 78

reproductive female birds and hypothesized to have existed in some non-avian 79

avemetatarsalians [18, 19]. This tissue is widely regarded as a short-term calcium store 80

available for shelling eggs [20, 21]. The authors summarize progress in diagnosing medullary 81

bone, while highlighting recent and emerging work on biochemical signatures, among other 82

important criteria, that support its recognition in fossils.

83

84

85

86

3. Thermometabolism 87

88

A section on the study of thermometabolism and thermoregulation reviews its physiological 89

mechanisms in vertebrates and palaeobiological inference within the extant phylogenetic 90

bracket of modern endotherms (i.e., birds and most mammal species). The acquisition of 91

endothermy—« metabolic heat production in the absence of muscular activity » [5]—is one of 92

the most significant innovations in vertebrate physiology. It modified the energetic 93

relationships between organisms and their environments [22], lifted constraints on external 94

thermal thresholds both temporally and spatially (e.g., diel activity patterns, latitudinal 95

gradients) [23], and likely coincided with a suite of changes in major organ systems involved in 96

respiration and circulation that prevail in the majority of terrestrially active (and many 97

secondarily aquatic) vertebrate species [24, 25]. At the ecosystem level, it imposed a 98

restructuring of animal communities along trophic webs [26]. The fossil record documents 99

major shifts in these biological systems spanning the Permian through Triassic periods, and 100

parsimony suggests that mammalian and avian endothermy evolved convergently—birds and 101

mammals are two distantly related tetrapod groups whose last common ancestor (ca. 320 Mya) 102

was most probably ectothermic.

103

Two thermogenetic mechanisms are analyzed in the theme issue. On the one hand, 104

mitochondria of brown adipose tissue produce heat by uncoupling food-derived substrate 105

oxidation from chemical energy (ATP) production in many eutherian mammals [27, 28]. It has 106

been shown that various physiological factors, including exercise, diet, and the immune system, 107

can cause the browning of white adipose tissue through epigenetic mechanisms [29]. In the 108

first contribution of this section, Jastroch & Seebacher [5] review the molecular mechanisms 109

underlying the browning of white adipocytes, and their potential contribution to endogenous 110

heat production in the evolution of endothermy. Bal and Perisamy [6] review another 111

mechanism of non-shivering thermogenesis: inhibition of Ca

transport, but not ATP 112

hydrolysis, of sarco-endoplasmic reticulum calcium ATPase (SERCA) by sarcolipin, resulting in 113

a futile pump activity that generates heat. The contribution by Legendre & Davesne [7] surveys 114

the homoplasic distribution of mechanisms involved in non-shivering thermogenesis across 115

vertebrate phylogeny. The authors argue that ‘endothermy’ in birds and mammals is often 116

inconsistently defined, and may represent evolutionarily labile mechanisms that permit 117

endogenous thermogenesis convergently in different clades.

118

Faure-Brac & Cubo [9] perform retrodictions of the thermometabolism of extinct 119

synapsids using phylogenetic eigenvector maps, a recently developed comparative method.

120

Based on a phylogenetic bracket of extant tetrapods, they establish a baseline relationship

121

6 between vascular histometrics in cortical bone and resting metabolic rate, and suggest that 122

some late Permian therapsids might have had resting metabolic rates comparable to extant 123

endothermic mammals exhibiting similar histology in contrast to more basal synapsids 124

(Varanopidae, Edaphosauridae, Ophiacodontidae). Prior studies have argued that other 125

vascular parameters, particularly canal sizes and densities that impact O

diffusive capacity, 126

reflected an expansion of aerobic scope in some Triassic therapsids and contemporary 127

archosauromorphs that may or may not have been coincident with changes in 128

thermoregulatory abilities [30]. The present authors conclude that palaeohistology reveals 129

independent acquisition of endotherm-like resting metabolic rates in at least three amniote 130

lineages: Therapsida, Sauropterygia, and Archosauromorpha [9]. Stable isotope 131

biogeochemistry helps to catalogue the fossil record of thermometabolism as a test of these 132

hypotheses. A previous analysis of the thermophysiology of marine reptiles showed that 133

Plesiosauria, Ichthyosauria and (probably) Mosasauridae were endotherms [31]. Results 134

obtained by Seon et al. [8] for Thalattoshuchia (marine crocodylomorphs) are consistent with 135

hydroxyapatite formed under temperatures intermediate between those of ectotherms and 136

endotherms, and behavioral adjustments are speculated to have played a role in their 137

thermoregulation.

138 139

4. Respiration and Cardiopulmonary Systems 140

141

Vertebrate respiratory and cardiopulmonary systems are specialized both for bulk convection 142

and diffusion of gases that make possible the elimination of CO

and uptake of O

for cellular 143

respiration. Modifications to these systems in the synapsid and archosaur lineages, which 144

include wide-ranging foragers and terrestrial cursors, likely promoted the expansion of aerobic 145

scope and athleticism previously unseen in vertebrates prior to the Permo-Triassic boundary.

146

Brocklehurst et al. [10] analyse the evolution of ventilation mechanics, as well as the 147

osteological correlates for lung structure and distribution of air sacs, in archosaurs.

148 149

5. Reproduction, Growth, and Life Cycle 150

151

Growth and reproduction are intricately linked to a variety of physiologic processes. For 152

instance, mammalian- and avian-style parental care and reproduction have been tied to the 153

very origins of endothermy [32, 33]. This is because selection for endothermy—whether 154

obligate or seasonally facultative [34]—permits the parent to maintain incubation 155

temperature, thereby promoting brood survival and fitness. Furthermore, endothermic

156

mammals and, especially, birds are known to be capable of relatively faster postnatal growth 157

than similar-sized ectotherms [35], possibly due to a combination of greater parental 158

investment during early growth, as well as resource use and metabolic processing. The 159

contributions of Canoville et al. [2], and Huttenlocker & Shelton [11], provide insights into early 160

growth and life cycle innovations of avian-line archosaurs and synapsids, respectively. In 161

addition to discussing the typology and histochemistry of medullary bone, Canoville et al.

162

promote its utility toward understanding more generally the fascinating reproductive biology 163

of dinosaurs [2]. Better characterization of medullary tissues in reproductive dinosaurs would 164

help palaeontologists identify sexual dimorphism in the fossil record, more accurately estimate 165

growth rate and age at maturity, and understand nesting and rearing behaviour. The transition 166

from aquatic tetrapods to more terrestrialized amniotes, such as basal synapsids, also brought 167

challenges that influenced innovations in growth and life cycle during the late Palaeozoic 168

establishment of land-based vertebrate communities. Huttenlocker & Shelton [11] present a 169

simple cross-sectional study showing prolonged, cyclic growth in basal synapsid limb bones, 170

and reduced bone robusticity reflective of a terrestrial life cycle freed from aquatic resources in 171

a predictable and seasonal climate regime.

172 173

6. Palaeopathology 174

175

While the following section could form the subject of a separate volume in its own right, the 176

conclusions of ‘palaeopathology’—the study of ancient disease—give inference to important 177

physiological and behavioural attributes of extinct animals that cannot otherwise be observed 178

directly. Whereas a vast literature exists on human skeletal disease, zoological palaeopathology 179

posits that knowledge of human disease is entirely inadequate to diagnose animal disease and 180

to explain the mechanisms of healing in vertebrate clades separated by millions of years of 181

evolution [36, 37]. For example, acute skeletal diseases in birds may be frequently 182

accompanied by granular or caseous abscesses because, unlike humans and other mammals, 183

they do not accumulate pus [38]. In this context, the contributions of Jentgen-Ceschino et al.

184

[12] and Kato et al. [13] explore the etiologies of reactive periosteal bone in three separate 185

cases in the archosaur and synapsid lineages, respectively. The exciting results of both studies 186

suggest avian- and mammal-like disease responses—rather than ‘reptile-like’—in extinct 187

dinosaurs and synapsids. Nonetheless, these cases highlight important caveats of cross-clade 188

comparisons and reinforce the need for ongoing sampling of fossil and extant baselines, multi- 189

modal data acquisition, and coordinated efforts by palaeopathologists to index these datasets 190

that could improve diagnostic rigour in fossils.

191

8 192

7. Synthesis: Inferring Physiological Capacities in Extinct Vertebrates 193

194

While elucidating the origins of physiological traits remains an important component of 195

evolutionary physiology, limitations endure that constrain our ability to reconstruct the 196

physiological capacities of extinct organisms with confidence. This is largely because ‘form’ can 197

be directly observed from fossilized tissues, whereas ‘function’ is inferred within a framework 198

of comparative anatomy, biophysics, and phylogenetic bracketing. Each requires reasonably 199

large comparative datasets (including extant training datasets), precision measurements, and 200

an accepted evolutionary model that is ratcheted to the fossil data (whether morphological, 201

histological, or biogeochemical). The final contributions of Gardner et al. [14] and Padian &

202

Ricqlès [15] address these theoretical limitations within quantitative and more philosophical 203

contexts. Gardner et al. [14] test the hypothesis of a causal relationship between genome size 204

and basal metabolic rate. This hypothesis is based on the postulate suggesting that nucleus size 205

(and cell size) may have an effect on cellular metabolism through, for example, surface area-to- 206

volume ratios or differences in GC content. The contributors did not find support for a direct 207

functional relationship between genome size and basal metabolic rate in extant vertebrates 208

using Bayesian phylogenetic statistical analysis [14]. The essay of Padian & Ricqles [15] offers a 209

critique of practical approaches to palaeophysiology. These approaches, the authors argue, are 210

limited to correlative factors inferred from fossilizable tissues under a modern framework that 211

encompasses only two binary categories—“cold-blooded” fishes, amphibians and reptiles, and 212

“warm-blooded” birds and mammals—which inadequately describe the breadth of 213

physiological strategies available to vertebrates. In addition to the large-scale phylogenetic 214

comparative studies such as those of Cubo et al. [39] and Gardner et al. [14], which attempt to 215

control for the effects of phylogeny, focused clade-specific studies that further control for body 216

size, age to maturity and growth rate, environmental context, and interelemental 217

histovariability (e.g., histovariation in Haversian replacement; [40]) shed further light on 218

physiologic capacities in extinct groups.

219 220

Acknowledgments 221

222

We thank the organizers of the 5

International Palaeontological Congress and all of the 223

contributing authors to the session “Vertebrate Palaeophysiology,” and, especially, to those who 224

contributed to this volume. We also thank our Senior Editor Helen Eaton.

225

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Author contributions 324

JC & AKH wrote the paper.

325 326

Competing interests 327

The authors declare no competing interests.

328 329

Short biographies 330

Jorge Cubo is a Professor of Palaeontology at Sorbonne University, Paris, France. He received 331

his PhD in bone biomechanics from the University of Barcelone, Spain, in 1997. His work 332

centres on palaeobiological inferences of thermometabolism in amniotes using bone histology 333

in a phylogenetic context. He has pioneered the utilisation of phylogenetic comparative 334

methods in comparative bone histology. Photography : © MNHN - Agnès Iatzoura 335

336

Adam Huttenlocker is an Assistant Professor of Integrative Anatomical Sciences at University of 337

Southern California, Los Angeles, USA. He received his PhD in palaeobiology from the 338

University of Washington, Seattle, in 2013, and from 2013–2016 held a prestigious National 339

Science Foundation Postdoctoral Fellowship at the University of Utah, Salt Lake City, to 340

investigate palaeophysiology and energetics in fossil tetrapods. His research combines 341

functional anatomy, medical imaging, and hard-tissue histology in order to understand skeletal 342

function, growth, and the origins of endothermic physiology in mammals and their extinct 343

synapsid forebears.

344