Metabolic heat production in archosaurs has played an important role in their evolutionary radiation during the Mesozoic, and their ancestral metabolic condition has long been a matter of debate in systematics and palaeontology. The study of fossil bone histology provides crucial information on bone growth rate, which has been used to indirectly investigate the evolution of thermometabolism in archosaurs. However, no quantitative estimation of metabolic rate has ever been performed on fossils using bone histological features. Moreover, to date, no inference model has included phylogenetic information in the form of predictive variables. Here we performed statistical predictive modeling using the new method of phylogenetic eigenvector maps on a set of bone histological features for a sample of extant and extinct vertebrates, to estimate metabolic rates of fossil archosauromorphs. This modeling procedure serves as a case study for eigenvector-based predictive modeling in a phylogenetic context, as well as an investigation of the poorly known evolutionary patterns of metabolic rate in archosaurs. Our results show that Mesozoic theropod dinosaurs exhibit metabolic rates very close to those found in modern birds, that archosaurs share a higher ancestral metabolic rate than that of extant ectotherms, and that this derived high metabolic rate was acquired at a much more inclusive level of the phylogenetic tree, among non-archosaurian archosauromorphs. These results also highlight the difficulties of assigning a given heat production strategy (i.e., endothermy, ectothermy) to an estimated metabolic rate value, and confirm findings of previous studies that the definition of the endotherm/ectotherm dichotomy may be ambiguous.
Endothermy, 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. This article is part of the theme issue ‘Vertebrate palaeophysiology’.
The presence of a phylogenetic signal in the variation of osteohistological features has been recently debated in the literature. Previous studies have found a significant signal for some features, but these results were obtained on a small amount of characters and a reduced sample. Here we perform a comprehensive study in which we quantify the phylogenetic signal on 62 osteohistological features in an exhaustive sample of palaeognathous birds. We used four different estimators to measure phylogenetic signal – Pagel's λ, Abouheif's Cmean, Blomberg's K, and Diniz‐Filho's phylogenetic eigenvector regressions PVR – and four topologies taken from the literature. Bone size and bone vascular density exhibit a strong phylogenetic signal, whereas all but four of the remaining features measured at the histological level – cellular size in caudal and medial transects of femora, and proportion of oblique vascular canals in rostral and caudal transects of tibiotarsi – exhibit a weaker signal. We also found that the impact of the topologies used in the analyses is very low compared with that of sample size. We conclude that the analysis of a comprehensive sample is crucial to obtain reliable quantifications of the phylogenetic signal. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112, 688–700.
Bone microstructure has long been known as a powerful tool to investigate lifestyle-related biomechanical constraints, and many studies have focused on identifying such constraints in the limb bones of aquatic or arboreal mammals in recent years. The limb bone microstructure of fossorial mammals, however, has not been extensively described. Furthermore, so far, studies on this subject have always focused on the bone histology of small burrowers, such as subterranean rodents or true moles. Physiological constraints associated with digging, however, are known to be strongly influenced by body size, and larger burrowers are likely to exhibit a histological profile more conspicuously influenced by fossorial activity. Here, we describe for the first time the limb bone histology of the aardvark (Orycteropus afer), the largest extant burrowing mammal. The general pattern is very similar for all six sampled limb bones (i.e., humerus, radius, ulna, femur, tibia, and fibula). Most of the cortex at midshaft is comprised of compacted coarse cancellous bone (CCCB), an endosteal tissue formed in the metaphyses through the compaction of bony trabeculae. Conversely, the periosteal bone is highly resorbed in all sections, and is reduced to a thin outer layer, suggesting a pattern of strong cortical drift. This pattern contrasts with that of most large mammals, in which cortical bone is of mostly periosteal origin, and CCCB, being a very compliant bone tissue type, is usually resorbed or remodeled during ontogeny. The link between histology and muscle attachment sites, as well as the influence of the semi-arid environment and ant-eating habits of the aardvark on its bone microstructure, are discussed. We hypothesize that the unusual histological profile of the aardvark is likely the outcome of physiological constraints due to both extensive digging behavior and strong metabolic restrictions. Adaptations to fossoriality are thus the result of a physiological compromise between limited food availability, an environment with high temperature variability, and the need for biomechanical resistance during digging. These results highlight the difficulties of deciphering all factors potentially involved in bone formation in fossorial mammals. Even though the formation and maintaining of CCCB through ontogeny in the aardvark cannot be unambiguously linked with its fossorial habits, a high amount of CCCB has been observed in the limb bones of other large burrowing mammals. The inclusion of such large burrowers in future histological studies is thus likely to improve our understanding of the functional link between bone growth and fossorial lifestyle in an evolutionary context.
signal in bone histology of amniotes revisited. -Zoologica Scripta, 00, 000-000. There is currently a debate about the presence of a phylogenetic signal in bone histological data, but very few rigorous tests have fuelled the discussions on this topic. Here, we performed new analyses using a larger set of seven histological traits and including 25 taxa (nine extinct and 16 extant taxa), using three methods: the phylogenetic eigenvector regression, the tree length distribution and the regressions on distance matrices. Our results clearly show that the phylogenetic signal in our sample of bone histological characters is strong, even after correcting for multiple testing. Most characters exhibit a significant phylogenetic signal according to at least one of our three tests, with the phylogeny often explaining 20-60% of the variation in the histological characters. Thus, we conclude that the phylogenetic comparative method should be systematically used in interspecific analyses of bone histodiversity to avoid problems of non-independence among observations. Corresponding authors: Michel Laurin, CNRS UMR 7207, MNHN, bâtiment de géologie. BC 45.
Birds share an array of unique characteristics among extant land vertebrates. Among these, external and microstructural characteristics of extant bird eggs have been linked to changes in reproductive strategy that arose among non‐avian theropod dinosaurs. More recently, differences in egg proportions recovered in crown birds relative to other dinosaurs were suggested as possibly linked to avian flight, but dense sampling close to its proposed origin was lacking. Here we assess the evolution of eggshell thickness in a targeted sample of 114 dinosaurs including birds, and test the relationship of eggshell thickness with potential life history correlates and locomotor mode using phylogenetic comparative methods. Only egg mass and flight are identified as significant predictors of eggshell thickness. While a high correlation between egg mass and eggshell thickness is expected, that relationship is much stronger in flying taxa, which show a significantly higher slope and lower residual variance than flightless species. This suggests stabilizing selection of eggshell thickness among theropods, as recovered for other traits in extant birds (e.g. genome size, metabolic rate). Within living birds, Eufalconimorphae present an apomorphic increase in relative eggshell thickness which remains unexplained, as few morphological synapomorphies of this clade have been identified.
Periosteal, endosteal, and intracortical blood vessels bring oxygen and nutrients to, and evacuate the metabolic by-products from, osteocytes. This vascular network is in communication with bone cells through a network of canaliculi containing osteocyte cytoplasmic processes. The geometric and physiological constraints involved in the relationships between osteocytes (including canaliculi) and blood vessels in bones remain poorly documented from a comparative point of view. Therefore, first of all we tested the first hypothesis (Hypothesis 1) that osteocytes in endotherms may have higher energetic expenditure and may produce more metabolic by-products than do osteocytes in ectotherms. For this, we tested and found evidence for the prediction, derived from this hypothesis, that the maximum absolute thickness of avascular bone tissue is significantly higher in lepidosaurs than in birds. We also tested two alternative hypotheses explaining the variation of bone vascular density in diapsids. The first of those (Hypothesis 2a) proposed that as body mass increases, the relative effectiveness of vascular supply of the periosteum decreases because its surface increases proportionally to the second power of bone length, whereas bone mass to be supplied increases proportionally to the third power. Accordingly, we predicted and found evidence that bone vascular density is directly related to bone size in both lepidosaurs and birds. The alternative hypothesis (Hypothesis 2b), suggesting that bone vascular density, like mass-specific resting metabolic rate, may decrease as body mass increases, was refuted by these last results. Knowledge of the cytological relationship between osteocytes and blood vessels in diapsids is poor. Here also we present preliminary results of a comparative cytological study on such a relationship.
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