Jorge Cubo

Sorbonne Université

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J. Castanet

Université Paris Cité

Armand de Ricqlès

Sorbonne Université

Emmanuel de Margerie

Ethologie animale et humaine

Lucas J. Legendre

The University of Texas at Austin

Adrià Casinos

Universitat de Barcelona

Paul Aubier

Sorbonne Université

Mathieu G. Faure‐Brac

Norsk Teknisk Museum

Mariana Valéria de Araújo Sena

Sorbonne Université

Vivian de Buffrénil

Centre National de la Recherche Scientifique

Stéphane Jouve

Centre National de la Recherche Scientifique

Cooperative Institutions

Centre National de la Recherche Scientifique

Sorbonne Université

Centre de recherche en paléontologie - Paris

Muséum national d'Histoire naturelle

Institut des Sciences de la Terre de Paris

Université Paris Cité

Structure et Instabilité des Génomes

Institut de Systématique, Évolution, Biodiversité

Institute of Paleoprimatology Human Paleontology Evolution and Paleoenvironments

Universitat de Barcelona

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Phylogenetic Signal in Bone Microstructure of Sauropsids

Systematic Biology (2005)

Jorge Cubo Fleur Ponton Michel Laurin Emmanuel de Margerie J. Castanet

In spite of the fact that the potential usefulness of bone histology in systematics has been discussed for over one and a half centuries, the presence of a phylogenetic signal in the variation of histological characters has rarely been assessed. A quantitative assessment of phylogenetic signal in bone histological characters could provide a justification for performing optimizations of these traits onto independently generated phylogenetic trees (as has been done in recent years). Here we present an investigation on the quantification of the phylogenetic signal in the following bone histological, microanatomical, and morphological traits in a sample of femora of 35 species of sauropsids: vascular density, vascular orientation, index of Haversian remodeling, cortical thickness, and cross-sectional area (bone size). For this purpose, we use two methods, regressions on distance matrices tested for significance using permutations (a Mantel test) and random tree length distribution. Within sauropsids, these bone microstructural traits have an optimal systematic value in archosaurs. In this taxon, a Mantel test shows that the phylogeny explains 81.8% of the variation of bone size and 86.2% of the variation of cortical thickness. In contrast, a Mantel test suggests that the phylogenetic signal in histological traits is weak: although the phylogeny explains 18.7% of the variation of vascular density in archosaurs, the phylogenetic signal is not significant either for vascular orientation or for the index of Haversian remodeling. However, Mantel tests seem to underestimate the proportion of variance of the dependent character explained by the phylogeny, as suggested by a PVR (phylogenetic eigenvector) analysis. We also deal with some complementary questions. First, we evaluate the functional dependence of bone vascular density on bone size by using phylogenetically independent contrasts. Second, we perform a variation partitioning analysis and show that the phylogenetic signal in bone vascular density is not a by-product of phylogentic signal in bone size. Finally, we analyze the evolution of cortical thickness in diapsids by using an optimization by squared change parsimony and discuss the functional significance of this character in terms of decreased buoyancy in crocodiles and mass saving in birds. These results are placed in the framework of the constructional morphology model, according to which the variation of a character in a clade has a historical (phylogenetic) component, a functional (adaptive) component, and a structural (architectural) component.

Phylogenetic comparative methods

Mantel test

10.1080/10635150591003461

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Citations (130)

Were Notosuchia (Pseudosuchia: Crocodylomorpha) warm-blooded? A palaeohistological analysis suggests ectothermy

Biological Journal of the Linnean Society (2020)

Jorge Cubo Mariana Valéria de Araújo Sena Paul Aubier Guillaume Houee Pénélope Claisse

Abstract Most Notosuchia were active terrestrial predators. A few were semi-aquatic, or were insectivorous, omnivorous or herbivorous. A question relative to their thermometabolism remains to be answered: were Notosuchia warm-blooded? Here we use quantitative bone palaeohistology to answer this question. Two variables were used as proxies to infer thermometabolism: resting metabolic rate and red blood cell dimensions. Resting metabolic rate was inferred using relative primary osteon area and osteocyte size, shape and density. Blood cell dimensions were inferred using harmonic mean canal diameter and minimum canal diameter. All inferences were performed using phylogenetic eigenvector maps. Both sets of analyses suggest that the seven species of Notosuchia sampled in this study were ectotherms. Given that extant Neosuchia (their sister group) are also ectotherms, and that archosaurs were primitively endotherms, parsimony suggests that endothermy may have been lost at the node Metasuchia (Notosuchia–Neosuchia) by the Early Jurassic. Semi-aquatic taxa such as Pepesuchus may have had thermoregulatory strategies similar to those of recent crocodylians, whereas the terrestrial taxa (Araripesuchus, Armadillosuchus, Iberosuchus, Mariliasuchus, Stratiotosuchus) may have been thermoregulators similar to active predatory varanids. Thermal inertia may have contributed to maintaining a stable temperature in large notosuchians such as Baurusuchus.

Ectotherm

Mammal

Sister group

Omnivore

Insectivore

10.1093/biolinnean/blaa081

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Citations (43)

H SP 90 Inhibition Causes Heterochronies in the Skull Ossification Sequences of Pleurodeles waltl (Urodela). Evolutionary Implications

HAL (Le Centre pour la Communication Scientifique Directe) (2019)

Miguel A. López‐Unzu Ana C. Durán Borja Fernández-Corujo Valentín Sans‐Coma Jorge Cubo

Universidad de Malaga. Campus de Excelencia Internacional Andalucia Tech. FPU15/03209, EST17/00194 and University of Malaga.

Pleurodeles

Source

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Testing gradual and speciational models of evolution in extant taxa: the example of ratites

Journal of Evolutionary Biology (2011)

Michel Laurin Sander W. S. Gussekloo David Marjanović Lucas J. Legendre Jorge Cubo

Abstract Ever since Eldredge and Gould proposed their model of punctuated equilibria, evolutionary biologists have debated how often this model is the best description of nature and how important it is compared to the more gradual models of evolution expected from natural selection and the neo‐Darwinian paradigm. Recently, Cubo proposed a method to test whether morphological data in extant ratites are more compatible with a gradual or with a speciational model (close to the punctuated equilibrium model). As shown by our simulations, a new method to test the mode of evolution of characters (involving regression of standardized contrasts on their expected standard deviation) is easier to implement and more powerful than the previously proposed method, but the Mesquite module comet (aimed at investigating evolutionary models using comparative data) performs better still. Uncertainties in branch length estimates are probably the largest source of potential error. Cubo hypothesized that heterochronic mechanisms may underlie morphological changes in bone shape during the evolution of ratites. He predicted that the outcome of these changes may be consistent with a speciational model of character evolution because heterochronic changes can be instantaneous in terms of geological time. Analysis of a more extensive data set confirms his prediction despite branch length uncertainties: evolution in ratites has been mostly speciational for shape‐related characters. However, it has been mostly gradual for size‐related ones.

Heterochrony

Character evolution

Punctuated equilibrium

10.1111/j.1420-9101.2011.02422.x

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Citations (16)

Bone histology of Iberosuchus macrodon (Sebecosuchia, Crocodylomorpha)

Lethaia (2017)

Jorge Cubo Meike Köhler Vivian de Buffrénil

Iberosuchus macrodon is a Cenozoic crocodyliform interpreted as a terrestrial, cursorial form. To assess whether this adaptation was accompanied by a high growth rate and an elevated resting metabolic rate (two features commonly attributed to several terrestrial Triassic Crocodylomorpha based on histology), we studied bone histology in the femora of two specimens attributed to I. macrodon. Beyond this question is the broader problem of the possible survival to the Cretaceous-Palaeogene extinction event of tachymetabolic sauropsids other than birds. At mid-diaphysis, bone cortices in Iberosuchus are made of a parallel-fibred tissue that turns locally to true lamellar bone. Cortical vascularization consists of simple longitudinal canals forming a network of medium density. The spacing pattern of conspicuous lines of arrested growth suggests asymptotic growth for Iberosuchus. This general histological structure prevails also in the metaphyseal region of the bones. It is basically similar to that encountered in certain large lizards adapted to active predation, the Varanidae and the Teidae. In one of the two Iberosuchus femora, however, an intracortical meniscus made of a tissue displaying a global radial architecture occurs in the region of the fourth trochanter. Histologically, the latter can be interpreted either as compacted spongiosa or as a fibro-lamellar complex with a gross radial orientation, a tissue corresponding to fast periosteal apposition. These observations suggest that Iberosuchus basically had a slow, cyclical growth indicative of an ecto-poikilothermic, lizard-like, resting metabolic rate. However, it might also have retained a limited capacity for fast periosteal accretion in relation to local morphogenetic requirements as, for instance, the development of crests or trochanters.

Histology

Cursorial

Apposition

Bone Growth

Diaphysis

10.1111/let.12203

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Citations (32)

Relationship between bone growth rate and the thickness of calcified cartilage in the long bones of the Galloanserae (Aves)

Journal of Anatomy (2005)

L. Montès Emmanuel de Margerie J. Castanet Armand de Ricqlès Jorge Cubo

The histological features of mineralized tissues can be preserved for hundreds of millions of years, and are therefore important potential sources of information for reconstructing the life history traits of extinct species. Bone growth rates and the duration of the growth period have recently been estimated in fossil archosaurs from periosteal ossification (a mechanism responsible for bone diametral growth). Similarly, data on endochondral ossification (the mechanism responsible for bone longitudinal growth) may also yield information on growth duration and rate among extinct vertebrates, as long as potentially informative structures are preserved. However, in order to carry out palaeobiological estimations of growth rate and/or the duration of growth, it is first necessary to quantify in extant species the relationship between these life history traits and the histological features of endochondral ossification that are potentially preserved in the fossil record. Here we analyse the ontogenetic variation of both bone longitudinal growth rate and the thickness of the calcified cartilage in the femora of two Galloanserae (Aves) and find a significant positive relationship between these variables in both species. We discuss possible factors underlying interspecific differences in this relationship, and conclude that it could be applied with caution to draw palaeobiological inferences.

Endochondral ossification

Bone Growth

Long bone

Fossil Record

10.1111/j.1469-7580.2005.00410.x

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Citations (14)

Palaeohistological Evidence for Ancestral High Metabolic Rate in Archosaurs

Systematic Biology (2016)

Lucas J. Legendre Guillaume Guénard Jennifer Botha Jorge Cubo

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.

Ectotherm

Phylogenetic comparative methods

Vertebrate paleontology

10.1093/sysbio/syw033

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Citations (115)

Wing bone laminarity in Pterosaurs: insights into torsional adaptations for flight evolution

Anais da Academia Brasileira de Ciências (2025)

Esaú Victor de Araújo Jorge Cubo Mariana Valéria de Araújo Sena Renan Alfredo Machado Bantim Luiz Carlos Weinschütz

Abstract Powered flight has evolved separately in three tetrapod clades: pterosaurs, birds (avian dinosaurs), and bats. To meet the challenges of powered flight, tetrapods acquired structural, mechanical, and physiological adaptations. Circumferential vascular canals, forming laminar bone, have been proposed to be an adaptation linked to withstanding torsional loading during flight in birds. However, whether laminarity serves as an indicator of biomechanical torsion in pterosaurs, remains to be elucidated. Through a comparative statistical approach, we investigate the association between cortical bone laminarity and skeletal stress in pterosaur flight. For the first time, the presence of laminarity in pterosaur bones was analyzed to observe torsion in bones associated with flight, using thirty-five thin sections of the tapejarid Caiuajara dobruskii, Anhangueridae, and Dsungaripteroidea pterosaurs. We conclude that adaptive relationships arise between bone microstructure and biomechanical function, with forelimb elements (humerus, ulna, and wing phalanges) exhibiting higher laminarity rates compared to hindlimb bones. Additionally, the results provide insights into the possible flight style of these pterosaurs through comparison with bird groups. The presence of laminarity in pterosaurs and birds, but not in bats, highlights that this feature, once considered exclusive to birds, may have convergently evolved in pterosaurs and birds.

10.1590/0001-3765202520240540

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Citations (0)

Pattern and process in constructional morphology

Evolution & Development (2004)

Jorge Cubo

Morphology

10.1111/j.1525-142x.2004.04018.x

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Citations (30)

Evidence for heterochrony in the evolution of the goshawk Accipiter gentilis (Accipitridae, Aves)

Annales des Sciences Naturelles - Zoologie et Biologie Animale (1999)