Ben Creisler
"Vertebrate Palaeophysiology" special issue with free pdfs
Philosophical Transactions of the Royal Society B 375(1793)
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Some papers to highlight:
General Theme
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0130Physiology 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 âretrodictâ) 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, acidâbase 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.
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0131The involvement of mineralized tissues in acidâbase homeostasis was likely important in the evolution of terrestrial vertebrates. Extant reptiles encounter hypercapnia when submerged in water, but early tetrapods may have experienced hypercapnia on land due to their inefficient mode of lung ventilation (likely buccal pumping, as in extant amphibians). Extant amphibians rely on cutaneous carbon dioxide elimination on land, but early tetrapods were considerably larger forms, with an unfavourable surface area to volume ratio for such activity, and evidence of a thick integument. Consequently, they would have been at risk of acidosis on land, while many of them retained internal gills and would not have had a problem eliminating carbon dioxide in water. In extant tetrapods, dermal bone can function to buffer the blood during acidosis by releasing calcium and magnesium carbonates. This review explores the possible mechanisms of acidâbase regulation in tetrapod evolution, focusing on heavily armoured, basal tetrapods of the Permo-Carboniferous, especially the physiological challenges associated with the transition to air-breathing, body size and the adoption of active lifestyles. We also consider the possible functions of dermal armour in later tetrapods, such as Triassic archosaurs, inferring palaeophysiology from both fossil record evidence and phylogenetic patterns, and propose a new hypothesis relating the archosaurian origins of the four-chambered heart and high systemic blood pressures to the perfusion of the osteoderms.
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0136Endothermy, i.e. the endogenous production of metabolic heat, has evolved multiple times among vertebrates, and several strategies of heat production have been studied extensively by physiologists over the course of the twentieth century. The independent acquisition of endothermy by mammals and birds has been the subject of many hypotheses regarding their origin and associated evolutionary constraints. Many groups of vertebrates, however, are thought to possess other mechanisms of heat production, and alternative ways to regulate thermogenesis that are not always considered in the palaeontological literature. Here, we perform a review of the mechanisms involved in heat production, with a focus on cellular and molecular mechanisms, in a phylogenetic context encompassing the entire vertebrate diversity. We show that endothermy in mammals and birds is not as well defined as commonly assumed by evolutionary biologists and consists of a vast array of physiological strategies, many of which are currently unknown. We also describe strategies found in other vertebrates, which may not always be considered endothermy, but nonetheless correspond to a process of active thermogenesis. We conclude that endothermy is a highly plastic character in vertebrates and provides a guideline on terminology and occurrences of the different types of heat production in vertebrate evolution.
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Jacob D. Gardner, Michel Laurin and Chris L. Organ (2020)
The relationship between genome size and metabolic rate in extant vertebrates
Philosophical Transactions of the Royal Society B 375(1793): Â20190146
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https://doi.org/10.1098/rstb.2019.0146https://royalsocietypublishing.org/doi/10.1098/rstb.2019.0146Free pdf:
https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0146Genome size has long been hypothesized to affect the metabolic rate in various groups of animals. The mechanism behind this proposed association is the nucleotypic effect, in which large nucleus and cell sizes influence cellular metabolism through surface area-to-volume ratios. Here, we provide a review of the recent literature on the relationship between genome size and metabolic rate. We also conduct an analysis using phylogenetic comparative methods and a large sample of extant vertebrates. We find no evidence that the effect of genome size improves upon models in explaining metabolic rate variation. Not surprisingly, our results show a strong positive relationship between metabolic rate and body mass, as well as a substantial difference in metabolic rate between endothermic and ectothermic vertebrates, controlling for body mass. The presence of endothermy can also explain elevated rate shifts in metabolic rate whereas genome size cannot. We further find no evidence for a punctuated model of evolution for metabolic rate. Our results do not rule out the possibility that genome size affects cellular physiology in some tissues, but they are consistent with previous research suggesting little support for a direct functional connection between genome size and basal metabolic rate in extant vertebrates.
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0147What can we know of the physiological regimes of ancient vertebrates? Essential to the exploration of this question are several epistemological tools: (i) a phylogenetic framework for interpreting whole animals and individual tissues, (ii) reliable knowledge of variation in populations and among climates and geographies, (iii) an understanding of phenotypic variation during ontogeny and between sexes, and (iv) a sense of the patterns of body size change, both phyletically and ontogenetically. Palaeobiologists are historically bound to a dichotomous set of terms developed long ago to describe the relatively depauperate living vertebrate fauna. This system sees only binary categories of five major groupings: the âcold-bloodedâ fishes, amphibians, and reptiles, and the âwarm-bloodedâ birds and mammals. The integration of histoanatomical data with patterns of size, growth and phylogeny provides an opportunity to re-imagine not only vertebrate palaeophysiology, but vertebrate physiology in general. Here, we discuss how four 'signals' or 'influences' on bone tissues--phylogeny, ontogeny, mechanics and environment--can help to address these questions.
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Archosaurs
Teleosauridae and Metriorhynchidae were thalattosuchian crocodylomorph clades that secondarily adapted to marine life and coexisted during the Middle to Late Jurassic. While teleosaurid diversity collapsed at the end of the Jurassic, most likely as a result of a global cooling of the oceans and associated marine regressions, metriorhynchid diversity was largely unaffected, although the fossil record of Thalattosuchia is poor in the Cretaceous. In order to investigate the possible differences in thermophysiologies between these two thalattosuchian lineages, we analysed stable oxygen isotope compositions (expressed as Î18O values) of tooth apatite from metriorhynchid and teleosaurid specimens. We then compared them with the Î18O values of coexisting endo-homeothermic ichthyosaurs and plesiosaurs, as well as ecto-poikilothermic chondrichthyans and osteichthyans. The distribution of Î18O values suggests that both teleosaurids and metriorhynchids had body temperatures intermediate between those of typical ecto-poikilothermic vertebrates and warm-blooded ichthyosaurs and plesiosaurs, metriorhynchids being slightly warmer than teleosaurids. We propose that metriorhynchids were able to raise their body temperature above that of the ambient environment by metabolic heat production, as endotherms do, but could not maintain a constant body temperature compared with fully homeothermic ichthyosaurs and plesiosaurs. Teleosaurids, on the other hand, may have raised their body temperature by mouth-gape basking, as modern crocodylians do, and benefited from the thermal inertia of their large body mass to maintain their body temperature above the ambient one. Endothermy in metriorhynchids might have been a by-product of their ecological adaptations to active pelagic hunting, and it probably allowed them to survive the global cooling of the Late Jurassic, thus explaining the selective extinction affecting Thalattosuchia at the JurassicâCretaceous boundary.
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0133Medullary bone (MB) is a sex-specific tissue produced by female birds during the laying cycle, and it is hypothesized to have arisen within Avemetatarsalia, possibly outside Avialae. Over the years, researchers have attempted to define a set of criteria from which to evaluate the nature of purported MB-like tissues recovered from fossil specimens. However, we argue that the prevalence, microstructural and chemical variability of MB in Neornithes is, as of yet, incompletely known and thus current diagnoses of MB do not capture the extent of variability that exists in modern birds. Based on recently published data and our own observations of MB distribution and structure using computed tomography and histochemistry, we attempt to advance the discourse on identifying MB in fossil specimens. We propose: (i) new insights into the phylogenetic breadth and structural diversity of MB within extant birds; (ii) a reevaluation and refinement of the most recently published list of criteria suggested for confidently identifying MB in the fossil record; (iii) reconsideration of some prior identifications of MB-like tissues in fossil specimens by taking into account the newly acquired data; and (iv) discussions on the challenges of characterizing MB in Neornithes with the goal of improving its diagnosis in extinct avemetatarsalians.
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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.
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The Archosauria are a highly successful group of vertebrates, and their evolution is marked by the appearance of diverse respiratory and metabolic strategies. This review examines respiratory function in living and fossil archosaurs, focusing on the anatomy and biomechanics of the respiratory system, and their physiological consequences. The first archosaurs shared a heterogeneously partitioned parabronchial lung with unidirectional air flow; from this common ancestral lung morphology, we trace the diverging respiratory designs of bird- and crocodilian-line archosaurs. We review the latest evidence of osteological correlates for lung structure and the presence and distribution of accessory air sacs, with a focus on the evolution of the avian lung-air sac system and the functional separation of gas exchange and ventilation. In addition, we discuss the evolution of ventilation mechanics across archosaurs, citing new biomechanical data from extant taxa and how this informs our reconstructions of fossils. This improved understanding of respiratory form and function should help to reconstruct key physiological parameters in fossil taxa. We highlight key events in archosaur evolution where respiratory physiology likely played a major role, such as their radiation at a time of relative hypoxia following the Permo-Triassic mass extinction, and their evolution of elevated metabolic rates.
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The histology of sauropod long bones often appears uniform and conservative along their evolutionary tree. One of the main aspects of their bone histology is to exhibit a fibrolamellar complex in the cortex of their long bones. Here, we report another bone tissue, the radial fibrolamellar bone (RFB), in the outer cortex of the humeri of a young adult cf. Isanosaurus (Early to Late Jurassic, Thailand) and an adult Spinophorosaurus nigerensis (Early to Middle Jurassic, Niger) that do not exhibit any pathological feature on the bone surface. Its location within the cortex is unexpected, because RFB is a rapidly deposited bone tissue that would rather be expected early in the ontogeny. A palaeopathological survey was conducted for these sampled specimens. Observed RFB occurrences are regarded as spiculated periosteal reactive bone, which is an aggressive form of periosteal reaction. A âhair-on-endâ pattern of neoplasmic origin (resembling a Ewing's sarcoma) is favoured for cf. Isanosaurus, while a sunburst pattern of viral or neoplasmic origin (resembling an avian osteopetrosis or haemangioma) is favoured for Spinophorosaurus. This study highlights the importance of bone histology in assessing the frequency and nature of palaeopathologies.
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Synapsids
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0138The acquisition of mammalian endothermy is poorly constrained both phylogenetically and temporally. Here, we inferred the resting metabolic rates (RMRs) and the thermometabolic regimes (endothermy or ectothermy) of a sample of eight extinct synapsids using palaeohistology, phylogenetic eigenvector maps (PEMs), and a sample of 17 extant tetrapods of known RMR (quantified using respirometry). We inferred high RMR values and an endothermic metabolism for the anomodonts (Lystrosaurus sp., Oudenodon bainii) and low RMR values and an ectothermic metabolism for Clepsydrops collettii, Dimetrodon sp., Edaphosaurus boanerges, Mycterosaurus sp., Ophiacodon uniformis and Sphenacodon sp. A maximum-likelihood ancestral states reconstruction of RMRs performed using the values inferred for extinct synapsids, and the values measured using respirometry in extant tetrapods, shows that the nodes Anomodontia and Mammalia were primitively endotherms. Finally, we performed a parsimony optimization of the presence of endothermy using the results obtained in the present study and those obtained in previous studies that used PEMs. For this, we assigned to each extinct taxon a thermometabolic regime (ectothermy or endothermy) depending on whether the inferred values were significantly higher, lower or not significantly different from the RMR value separating ectotherms from endotherms (1.5 ml O2 hâ1 gâ0.67). According to this optimization, endothermy arose independently in Archosauromorpha, Sauropterygia and Therapsida.
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https://royalsocietypublishing.org/doi/pdf/10.1098/rstb.2019.0142Varanopids were a group of small to medium-sized synapsids whose fossil record spans the Carboniferous through middle Permian. Although their phylogenetic relationships have received some interest in recent years, little is known about other aspects of their palaeobiology, including their skeletal growth, allometry and habitat preference. Here, we describe varanopid long bone histology based on a sample of well-preserved femora from the lower Permian Richards Spur fissure fill locality, Comanche County, Oklahoma, USA. The sample includes five femora from at least two varanopid taxa--Mycterosaurus and the large varanodontine Varanops brevirostris--and four additional mycterosaurine femora not diagnosed to genus. Prior work on femoral bone compactness provided a baseline to make lifestyle inferences and evaluate whether varanopids were ancestrally terrestrial. Moreover, the large availability of specimens spanning different sizes made possible an assessment of size-related ontogenetic histovariability. All specimens revealed moderately dense cortical bone tissues composed of sparsely vascularized parallel-fibred and lamellar bone with radially arranged rows of longitudinal canals (mostly simple), and many preserved regularly spaced growth marks (annuli and lines of arrested growth) as in modern varanids. We show that bone histology has the potential to explain how ballast was shed and the skeleton lightened for terrestrial mobility in ancestral synapsids and their basal amniote kin, as well as how adjustments in postnatal growth influenced the evolution of larger body sizes in the terrestrial frontier.
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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.
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